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The New Red Algal Subphylum Proteorhodophytina Comprises the Largest and Most Divergent Plastid Genomes Known
Abstract and Figures
Red algal plastid genomes are often considered ancestral and evolutionarily stable, and thus more closely resembling the last common ancestral plastid genome of all photosynthetic eukaryotes [1, 2]. However, sampling of red algal diversity is still quite limited (e.g., [2, 3, 4, 5]). We aimed to remedy this problem. To this end, we sequenced six new plastid genomes from four undersampled and phylogenetically disparate red algal classes (Porphyridiophyceae, Stylonematophyceae, Compsopogonophyceae, and Rhodellophyceae) and discovered an unprecedented degree of genomic diversity among them. These genomes are rich in introns, enlarged intergenic regions, and transposable elements (in the rhodellophycean Bulboplastis apyrenoidosa), and include the largest and most intron-rich plastid genomes ever sequenced (that of the rhodellophycean Corynoplastis japonica; 1.13 Mbp). Sophisticated phylogenetic analyses accounting for compositional heterogeneity show that these four “basal” red algal classes form a larger monophyletic group, Proteorhodophytina subphylum nov., and confidently resolve the large-scale relationships in the Rhodophyta. Our analyses also suggest that secondary red plastids originated before the diversification of all mesophilic red algae. Our genomic survey has challenged the current paradigmatic view of red algal plastid genomes as “living fossils” [1, 2, 6] by revealing an astonishing degree of divergence in size, organization, and non-coding DNA content. A closer look at red algae shows that they comprise the most ancestral (e.g., [2, 7, 8]) as well as some of the most divergent plastid genomes known.
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... The subphylum Eurhodophytina comprises the Bangiophyceae and Florideophyceae, the classes containing seaweeds, whereas the unicellular and extremophilic Cyanidiophyceae solely form the subphylum Cyanidiophytina, sister to the rest of red algae (Qiu et al. 2016). The placement of the remaining four classes (Porphyridiophyceae, Compsopogonophyceae, Rhodellophyceae, and Stylonematophyceae) was long unclear before a phylogenetic study including a representative taxon sampling showed that they were monophyletic and proposed the subphylum Proteorhodophytina to host them (Muñoz-Gómez et al. 2017). ...
... Among them, the plastid genomes (plastomes) of red algae are usually thought to retain several primitive features and to evolve slowly (Butterfield 2000;Glöckner et al. 2000;Janouškovec et al. 2013). For example, plastome alignments within the classes Bangiophyceae and Florideophyceae show little change in synteny (Janouškovec et al. 2013;Cao et al. 2018), although Cyanidiaceae and inter-class comparisons show less conservation (Janouškovec et al. 2013;Muñoz-Gómez et al. 2017). Genome size shows little variation as well, typically ranging from 150 to 200 kb. ...
... Genome size shows little variation as well, typically ranging from 150 to 200 kb. By contrast, intron invasion has resulted in massive plastome expansion in the Proteorhodophytina: the Rhodellophyceae include the largest red algal plastid genome (1.1 Mb in Corynoplastis japonica), more than five times larger than the typical florideophyte plastomes (Muñoz-Gómez et al. 2017). ...
Proliferation of selfish genetic elements has led to significant genome size expansion in plastid and mitochondrial genomes of various eukaryotic lineages. Within the red algae, such expansion events are only known in the plastid genomes of the Proteorhodophytina, a highly diverse group of mesophilic microalgae. By contrast, they have never been described in the much understudied red algal mitochondrial genomes. Therefore, it remains unclear how widespread such organellar genome expansion events are in this eukaryotic phylum. Here, we describe new mitochondrial and plastid genomes from 25 red algal species, thereby substantially expanding the amount of organellar sequence data available, especially for Proteorhodophytina, and show that genome expansions are common in this group. We confirm that large plastid genomes are limited to the classes Rhodellophyceae and Porphyridiophyceae, which in part are caused by lineage-specific expansion events. Independently expanded mitochondrial genomes - up to three times larger than typical red algal mitogenomes - occur across Proteorhodophytina classes and a large shift towards high GC content occurred in the Stylonematophyceae. Although intron proliferation is the main cause of plastid and mitochondrial genome expansion in red algae, we do not observe recent intron transfer between different organelles. Phylogenomic analyses of mitochondrial and plastid genes from our expanded taxon sampling yielded well-resolved phylogenies of red algae with strong support for the monophyly of Proteorhodophytina. Our work shows that organellar genomes followed different evolutionary dynamics across red algal lineages.
... Most of the biodiversity studies on red algae have been focussed on the mesophilic seaweeds of the subphylum Eurhodophytina and on the unicellular thermoacidophilic members of the subphylum Cyanidiophytina, whereas the recently recognized subphylum Proteorhodophytina has been less investigated (Verbruggen et al. 2010;Muñoz-Gómez et al. 2017). This subphylum includes several classes, some containing many unicellular members and one with only unicellular representatives, the Rhodellophyceae. ...
... Moreover, often microalgal taxa have a wide distribution, but the crypticity of the diverse entities does not allow their distinction just based on morphology (e.g. Zuccarello et al. 2008;Necchi et al. 2013) and the scarce sampling for certain groups (Verbruggen et al. 2010;Muñoz-Gómez et al. 2017) hinders the recognition of both known and new species. ...
... For the 18S rRNA gene, a dataset was created including the newly obtained sequences and other suitable sequences available in the INSDC repositories, following the most recent classifications (Yoon et al. 2006;Yokoyama et al. 2009;Scott et al. 2011;Muñoz-Gómez et al. 2017). Representative sequences of the class Rhodellophyceae were included, as well as of the allied classes Compsopogonophyceae, Stylonematophyceae, Porphyridiophyceae and Bangiophyceae. ...
During samplings aimed at isolating microalgal strains, a coccoid greyish-green alga was collected along the North Adriatic coasts (Mediterranean Sea, Italy) and grown in culture. The microalgal strain (named strain B1A) was then subjected to an integrative taxonomy approach in order to correctly identify it. Morphological and ultrastructural observations and phycobiliprotein content analysis were carried out, as well as molecular analyses based on the 18S rRNA, rbcL, psbA and plastid-encoded 23S rRNA genes. Phylogenetic placement and ultrastructural observations clearly indicated that strain B1A is a member of the red microalgal genus Dixoniella (Rhodellophyceae, Proteorhodophytina) and is distinct from the only species so far described for this taxon. Therefore, a new species was described to encompass the isolate from the North Adriatic Sea and another isolate from Japan (MF-G2), which was phylogenetically related to strain B1A: Dixoniella giordanoi sp. nov.
... Due to the multicellular members of the Bangiophyceae and the entirely multicellular Florideophyceae, secondary gains of complexity (after the genome reduction event) are evident in both latter lineages. The tree as well as the timeline are based on a recently published molecular clock analysis [2] and comprehensive phylogenetic analyses [25,26]. The nodes within the phylogeny are placed according to the data split times (see bottom timeline), and the position of the cartoons of the analyzed species represent the first split within the respective lineage. ...
... The clustering of Pyropia yezoensis was adapted so that the two Bangiophyceae form a clade. In addition, the clustering of Porphyridium purpureum was modified according to the phylogeny of Muñoz-Gómez et al. [25], resulting in the Porphyridiophyceae representing a sister lineage to the Florideophyceae and Bangiophyceae clade [25]. Since C. merolae was the only species in the tree for the Cyanidiales, the branch lengths for Galdieria phlegrea and Galdieria sulphuraria were taken from Qiu et al. [42] and were adjusted and set in relation to the branch length from the species tree reported by Leebens-Mack et al. [26]. ...
... The clustering of Pyropia yezoensis was adapted so that the two Bangiophyceae form a clade. In addition, the clustering of Porphyridium purpureum was modified according to the phylogeny of Muñoz-Gómez et al. [25], resulting in the Porphyridiophyceae representing a sister lineage to the Florideophyceae and Bangiophyceae clade [25]. Since C. merolae was the only species in the tree for the Cyanidiales, the branch lengths for Galdieria phlegrea and Galdieria sulphuraria were taken from Qiu et al. [42] and were adjusted and set in relation to the branch length from the species tree reported by Leebens-Mack et al. [26]. ...
Red algae (Rhodophyta) belong to the superphylum Archaeplastida, and are a species-rich group exhibiting diverse morphologies. Theory has it that the unicellular red algal ancestor went through a phase of genome contraction caused by adaptation to extreme environments. More recently, the classes Porphyridiophyceae, Bangiophyceae, and Florideophyceae experienced genome expansions, coinciding with an increase in morphological complexity. Transcription-associated proteins (TAPs) regulate transcription, show lineage-specific patterns, and are related to organismal complexity. To better understand red algal TAP complexity and evolution, we investigated the TAP family complement of uni- and multi-cellular red algae. We found that the TAP family complement correlates with gain of morphological complexity in the multicellular Bangiophyceae and Florideophyceae, and that abundance of the C2H2 zinc finger transcription factor family may be associated with the acquisition of morphological complexity. An expansion of heat shock transcription factors (HSF) occurred within the unicellular Cyanidiales, potentially as an adaption to extreme environmental conditions.
... Nearly all plastid genomes consist of a single circular-mapping chromosome, typically between 100 and 200 kb and encoding circa 80-250 genes [4,6]. Diversity in size, gene content, density, and organization of plastid genomes among different eukaryotic lineages [7][8][9] is by and large limited, especially when compared to mitochondria. ...
... Currently, and in stark contrast to other algae [9,[24][25][26], little is known about the gene content and structure of the chloroplast genome in the Cladophorales (Ulvophyceae), an ecologically important group of marine and freshwater green algae, which includes several hundreds of species. These macroscopic multicellular algae have giant, multinucleate cells containing numerous chloroplasts ( Figures 1A-1C). ...
... These values are concordant with the high density of the LMW fraction observed in CsCl/bisbenzimide gradients [29], and also with sequence data from cloned plasmids of Ernodesmis (51%-59% GC) [31]. Plastid genomes are generally AT rich and, in green algal species, GC content typically ranges between 26% and 43% [9,37]. GC-rich plastid genomes are very rare, but higher values have been reported for the trebouxiophycean green algae Coccomyxa subellipsoidea, Paradoxia multiseta (both 51% GC), and total-RNA assemblies. ...
Virtually all plastid (chloroplast) genomes are circular double-stranded DNA molecules, typically between 100-200 kb in size and encoding circa 80-250 genes. Exceptions to this universal plastid genome architecture are very few and include the dinoflagellates where genes are located on DNA minicircles. Here we report on the highly deviant chloroplast genome of Cladophorales green algae, which is entirely fragmented into hairpin plasmids. Short and long read high-throughput sequencing of DNA and RNA demonstrated that the chloroplast genes of Boodlea composita are encoded on 1-7 kb DNA contigs with an exceptionally high GC-content, each containing a long inverted repeat with one or two protein-coding genes and conserved non-coding regions putatively involved in replication and/or expression. We propose that these contigs correspond to linear single-stranded DNA molecules that fold onto themselves to form hairpin plasmids. The Boodlea chloroplast genes are highly divergent from their corresponding orthologs. The origin of this highly deviant chloroplast genome likely occurred before the emergence of the Cladophorales, and coincided with an elevated transfer of chloroplast genes to the nucleus. A chloroplast genome that is composed only of linear DNA molecules is unprecedented among eukaryotes and highlights unexpected variation in the plastid genome architecture.
... Given that the three different genes in this study exhibited distinct evolutionary histories for species within Corallina, concatenation was deemed inappropriate for determining phylogenetic relationships and the partially concatenated tree (Fig. S1) was included to illustrate how misleading conclusions may result from concatenation. Furthermore, assuming that each mitochondrial and plastid genome consists of one uniparentally inherited chromosome, congruence would at least be expected between individual mitochondrial or plastid gene genealogies (Janouškovec et al. 2013;Muñoz-Gómez et al. 2017;Lee et al. 2018;Yoshida & Mogi 2019). The discovery of incongruence between the psbA and rbcL plastid genes, presumably located on the same chromosome, was therefore unexpected. ...
... This study corroborates recent findings by Yesson et al. (2020), in which mitochondrial and plastid genome phylogenies of C. officinalis differed. Other studies of red algal genomes have reported high genomic diversity, transposons, and evidence of horizontal gene transfer and parasitic genetic elements (Janouškovec et al. 2013;Lee et al. 2016;Muñoz-Gómez et al. 2017). Potential causes of such patterns include hybridization or incomplete lineage sorting, particularly among early-diverged lineages after rapid radiation (Lee et al. 2016(Lee et al. , 2018Tavares et al. 2018), perhaps lending insight into the evolutionary history of Corallina species. ...
To determine whether Corallina chilensis is a distinct species or a variety (i.e. C. officinalis var. chilensis) of the generitype of Corallina, molecular phylogenetic analyses were performed using psbA, COI-5P, rbcL, or some combination of these gene regions from 75 voucher specimens representing Corallina collections from around the world. Names were applied by comparing these DNA sequences with sequences obtained from type specimens, including a 263 bp rbcL sequence from an isotype of C. chilensis collected by Darwin (C. Darwin 2151) from Valparaiso, Chile. DNA sequences from the C. chilensis isotype matched unnamed coralline DNA sequences from British Columbia, Canada, and previously published DNA sequences from the northeast and southeast Pacific. The clade containing the isotype of C. chilensis was distinct from C. officinalis specimens in phylogenetic analyses. Although morphologically variable, fronds of C. chilensis from British Columbia populations matched Kützing's original description of C. officinalis var. chilensis. These data support the conclusion that C. chilensis is a distinct species, not a variety of C. officinalis, and is distributed in both hemispheres. While this study strongly supported C. chilensis as a distinct species, phylogenetic relationships among Corallina species remain elusive because individual gene trees are not congruent.
... In chronological order, the changes proposed were: Sheathia, former section Helminthoidea Phylogenomic studies of freshwater red algae are still relatively scarce but few mitochondrial and plastid genomes have been published recently. Muñoz-Gómez et al. (2017) included Boldia and Compsopogon in a study of chloroplast genome size in the Proteorhodophytina. Likewise, Lee et al. (2016) published the chloroplast genome of Thorea hispida as part of a more general study on the plastid genome architecture of red seaweeds and seed plants and Nan et al. (2017) compared the organelle genomes of a member of the Compsopogonales, Thoreales, and Batrachospermales to analyze their architecture and gene content features. ...
... Therefore, the classification is primarily based on morphology and information about phylogenetic relationships among these genera is limited. However, a study of the chloroplast genomes within the subphylum has provided the largest known chloroplast genomes and revealed a great range in chloroplast size among members sequenced (Muñoz-Gómez et al. 2017). Findings such as these will most likely spark more studies that will also help clarify the systematics within the subphylum and among genera. ...
A brief history of freshwater red algal studies is provided with a focus on researchers who wrote early treatises on cryptogams, those who pioneered studies focused on freshwater red algal taxonomy, research on freshwater red algae in several parts of the world and studies that applied new types of evidence for systematics research. Our current knowledge of the taxonomic diversity of freshwater red algae and their phylogenetic relationships is summarized. The biogeography of some macroscopic taxa is briefly discussed. Guidance is provided on procedures, equipment, and tools for collection and preservation of freshwater red algae. Information on the taxonomic scope and organization of this book is presented.
... The two putative serC genes are intact and not pseudogenes [18].The genome contains a single intron, a group II intron in psaA with a 515 amino-acid long ORF coding for a putative reverse transcriptase. Similar introns in the same gene have been previously identified in various microalgae such as the diatoms Toxarium undulatum Bailey 1854 (AOS86555) [16] and Haslea silbo Gastineau, Hansen and Mouget 2021 (QUS63628 and QUS63831) [19], the silicoflagellate Dictyocha speculum Ehrenberg 1839 (QDH81707) [20], the red alga Bulboplastis apyrenoidosa A.Kushibiki, A.Yokoyama, M.Iwataki, J.Yokoyama, J.A.West & Y.Hara 2012 (ARO90857) [21], and the green alga Chlamydomonas applanata Pringsheim 1930 (ALO63257) [22]. The best blastp hit (62.02% identity and E-value = 0.0) was obtained with the D. speculum intron-encoded protein. ...
... The two putative serC genes are intact and not pseudogenes [18].The genome contains a single intron, a group II intron in psaA with a 515 amino-acid long ORF coding for a putative reverse transcriptase. Similar introns in Mouget 2021 (QUS63628 and QUS63831) [19], the silicoflagellate Dictyocha speculum Ehrenberg 1839 (QDH81707) [20], the red alga Bulboplastis apyrenoidosa A.Kushibiki, A.Yokoyama, M.Iwataki, J.Yokoyama, J.A.West & Y.Hara 2012 (ARO90857) [21], and the green alga Chlamydomonas applanata Pringsheim 1930 (ALO63257) [22]. The best blastp hit (62.02% identity and E-value = 0.0) was obtained with the D. speculum intron-encoded protein. ...
We sequenced the plastid genomes of three diatoms from the genus Climaconeis, including
two strains formerly designated as Climaconeis scalaris. At 208,097 and 216,580 bp, the plastid genomes
of the latter strains are the largest ever sequenced among diatoms and their increased size is explained
by the massive expansion of the inverted repeat region. Important rearrangements of gene order
were identified among the two populations of Climaconeis cf. scalaris. The other sequenced Climaconeis
chloroplast genome is 1.5 times smaller compared with those of the Climaconeis cf. scalaris strains and
it features an usual quadripartite structure. The extensive structural changes reported here for the
genus Climaconeis are compared with those previously observed for other algae and plants displaying
large plastid genomes.
... The results of our phylogenetic analysis (Fig. S3) and the position of the cysT and cysW genes in the Olisthodiscus plastid genome being conserved with those seen in cyanidiophytes (Fig. S4) provide strong evidence that these two genes were passed vertically from a red algal ancestor of the Olisthodiscus plastid. Given phylogenetic evidence for the common ancestry of plastids in all ochrophytes, haptophytes, cryptophytes, and the Myzozoa subgroup of Alevolata, that is "chromalveolates" ( Sev c ıkov a et al. 2015, Muñoz-G omez et al. 2017, all these groups, except Olisthodiscus, must lack cysT and cysW as a result of multiple losses. Furthermore, since the red algal ancestor of the "chromalveolate" plastids belonged to a lineage that branched off in the red algal phylogeny only after the divergence of Cyanidiophyceae (Muñoz-G omez et al. 2017), cysT and cysW were most likely lost only before the radiation of the "core" rhodophytes (i.e., subphyla Proteorhodophytina and Eurhodophytina). ...
... Given phylogenetic evidence for the common ancestry of plastids in all ochrophytes, haptophytes, cryptophytes, and the Myzozoa subgroup of Alevolata, that is "chromalveolates" ( Sev c ıkov a et al. 2015, Muñoz-G omez et al. 2017, all these groups, except Olisthodiscus, must lack cysT and cysW as a result of multiple losses. Furthermore, since the red algal ancestor of the "chromalveolate" plastids belonged to a lineage that branched off in the red algal phylogeny only after the divergence of Cyanidiophyceae (Muñoz-G omez et al. 2017), cysT and cysW were most likely lost only before the radiation of the "core" rhodophytes (i.e., subphyla Proteorhodophytina and Eurhodophytina). ...
The phylogenetic diversity of Ochrophyta, a diverse and ecologically important radiation of algae, is still incompletely understood even at the level of the principal lineages. One taxon that has eluded simple classification is the marine flagellate genus Olisthodiscus. We investigated O. luteus K‐0444, and documented its morphological and genetic differences from the NIES‐15 strain, which we described as O. tomasii sp. nov. Phylogenetic analyses of combined 18S and 28S rRNA sequences confirmed that Olisthodiscus constitutes a separate, deep, ochrophyte lineage, but its position could not be resolved. To overcome this problem, we sequenced the plastid genome of O. luteus K‐0444 and used the new data in multigene phylogenetic analyses, which suggested that Olisthodiscus is a sister lineage of the class Pinguiophyceae within a broader clade additionally including Chrysophyceae, Synchromophyceae, and Eustigmatophyceae. Surprisingly, the Olisthodiscus plastid genome contained three genes, ycf80, cysT, and cysW, inherited from the rhodophyte ancestor of the ochrophyte plastid yet lost from all other ochrophyte groups studied so far. Combined with nuclear genes for CysA and Sbp proteins, Olisthodiscus is the only known ochrophyte possessing a plastidial sulfate transporter SulT. In addition, the finding of a cemA gene in the Olisthodiscus plastid genome and an updated phylogenetic analysis ruled out the previously proposed hypothesis invoking horizontal cemA transfer from a green algal plastid into Synurales. Altogether, Olisthodiscus clearly represents a novel phylogenetically distinct ochrophyte lineage, which we have proposed as a new class, Olisthodiscophyceae.
... The largest chloroplast genome ever sequenced has very recently been found in the red algae Corynoplastis japonica. Its genome size goes up to 1 Mb and contains 209 genes [24]. On average, the largest plastomes are found in the Rhodophyta with an average size of about 183 kb (minimum = 149,987 kb, maximum = 610,063 kb, excluding the small 90 kb genome of the parasite of C. polysiphoniae), whereas Glaucophyta and Streptophyta have an average chloroplast genome size of between 130 and 160 kb (minimum = 107,236 kb; maximum = 242,575 kb, excluding the parasitic and non-chlorophyll species), respectively ( Table 1). ...
... Several factors can explain the important size variations found among the Archaeplastida. In the case of the red algae C. japonica and Bulboplastis apyrenoidosa (more than 1 Mb and 600 kb long plastomes, respectively), the increase of plastome size is due to an expansion of the intron number with more than 200 introns found in these species [24]. In Angiosperms, plastome variations have been observed but in a lesser extent. ...
Photosynthetic eukaryotic cells arose more than a billion years ago through the engulfment of a cyanobacterium that was then converted into a chloroplast, enabling plants to perform photosynthesis. Since this event, chloroplast DNA has been massively transferred to the nucleus, sometimes leading to the creation of novel genes, exons, and regulatory elements. In addition to these evolutionary novelties, most cyanobacterial genes have been relocated into the nucleus, highly reducing the size, gene content, and autonomy of the chloroplast genome. In this chapter, we will first present our current knowledge on the origin and evolution of the plant plastome in the different Archaeplastida lineages (Glaucophyta, Rhodophyta, and Viridiplantae), focusing on its gene content, genome size, and structural evolution. Second, we will present the factors influencing the rate of DNA transfer from the chloroplast to the nucleus, the evolutionary fates of the nuclear integrants of plastid DNA (nupts) in their new eukaryotic environment, and the drivers of chloroplast gene functional relocation to the nucleus. Finally, we will discuss how cytonuclear interactions led to the intertwined coevolution of nuclear and chloroplast genomes and the impact of hybridization and allopolyploidy on cytonuclear interactions
... These studies have resolved numerous phylogenetic controversies, deepening our understanding of life's history (Capella-Gutiérrez et al. 2012;King and Rokas 2017;Williams et al. 2019;Pipes et al. 2021;Steenwyk et al. 2023a). Phylogenomics has also proven useful for delineating lineage relationships at taxonomic scales ranging from species to higher-order relationships (Muñoz-Gómez et al. 2017;Díaz-Tapia et al. 2017;Mateo-Estrada et al. 2019;Bringloe et al. 2021;Steenwyk et al. 2022b;Sierra-Patev et al. 2023). Species trees inferred using phylogenomics provide the framework for various comparative evolutionary genomic studies, such as determining gene duplication and loss events or studying phenotypic innovation (Zhang et al. 2014b;Steenwyk et al. 2019a;Fernández and Gabaldón 2020;Shen et al. 2020;Phillips et al. 2021;Li et al. 2022b;Opulente et al. 2023;Title et al. 2024). ...
Phylogenomics has enriched our understanding that the Tree of Life can have network-like or reticulate structures among some taxa and genes. Non-vertical modes of evolution—such as hybridization/introgression and horizontal gene transfer—deviate from a strictly bifurcating tree model, causing non-treelike patterns. Here, we present a brief overview of a phylogenomic workflow for inferring organismal histories and compare methods for detecting reticulate evolution. We discuss how the timing of coalescent events can help disentangle introgression from incomplete lineage sorting and how horizontal gene transfer events can help determine the relative timing of speciation events. In doing so, we identify pitfalls of certain methods and discuss how to extend their utility across the Tree of Life. Workflows, methods, and future directions discussed herein underscore the need to embrace reticulate evolutionary patterns for understanding the timing and rates of evolutionary events, providing a clearer understanding of life’s history.
... Moreover, organelle genome databases provide valuable insights into the phylogenetic relationships and molecular evolution of various species. For example, mitochondrial and chloroplast genome data have been crucial in reestablishing the phylogenetic relationships among red algae [15][16][17] . ...
Pyropia is a genus comprising red algae of the Bangiaceae family that is commonly found in intertidal zones worldwide. However, understanding of Pyropia species that are prone to tropical regions remains limited despite recent breakthroughs in genomic research. Within the realm of Pyropia species thriving in tropical regions, P. vietnamensis stands out as a widely recognized species. In this study, we aimed to investigate Pyropia species in the southwest coast of Myanmar using physiological and molecular approaches, culture-based analyses, chloroplast rbcL and nuclear SSU gene sequencing, and whole chloroplast and mitochondrial genome sequencing. Physiological analysis showed that the Myanmar samples were more heat-tolerant than their Japanese counterparts, including those of subtropical origin. Additionally, molecular characterization revealed that the Myanmar samples were closely related to P. vietnamensis from India. This study is the first to sequence the chloroplast and mitochondrial genomes of Pyropia species from tropical regions. A unique deletion event was observed within a ribosomal RNA gene cluster in the chloroplast genome of the studied Pyropia species, which is a deviation from the usual characteristics of most Pyropia species. This study improves current understanding of the physiological and molecular characteristics of this comparatively understudied Pyropia species that grows in tropical regions.
... The Florideophyceae have complex branched thalli that are often pseudoparenchymatous with distinctive reproductive structures (discussed below), whereas the Bangiophyceae have a much simpler organisation, lacking distinct morphological features that rendered their classification more challenging. Molecular phylogenies have confirmed this traditional taxonomic separation and have grouped these two multicellular classes together in the subphyllum Eurhodophytina ( Fig. 1), with the Bangiophyceae assemblage appearing to have paraphyletic origins (Yoon et al., 2006;Verbruggen et al., 2010;Qiu, 2016;Muñoz-G omez et al., 2017;Van Beveren et al., 2022). The other two Rhodophyta subphyla correspond to divergent ancient lineages that arose at the beginning of the Mesoproterozoic (c. ...
Rhodophyta (or red algae) are a diverse and species‐rich group that forms one of three major lineages in the Archaeplastida, a eukaryotic supergroup whose plastids arose from a single primary endosymbiosis. Red algae are united by several features, such as relatively small intron‐poor genomes and a lack of cytoskeletal structures associated with motility like flagella and centrioles, as well as a highly efficient photosynthetic capacity. Multicellular red algae (or macroalgae) are one of the earliest diverging eukaryotic lineages to have evolved complex multicellularity, yet despite their ecological, evolutionary, and commercial importance, they have remained a largely understudied group of organisms. Considering the increasing availability of red algal genome sequences, we present a broad overview of fundamental aspects of red macroalgal biology and posit on how this is expected to accelerate research in many domains of red algal biology in the coming years.
... MtDNA encodes 5 to 100 genes, which play a role in oxidative phosphorylation, protein synthesis, protein transport and maturation, RNA processing, and in some rare instances, transcription (Lavrov and Lang, 2013). PtDNAs encode the same types of genes plus those involved in photosynthesis, summing up to as many as 250 genes (Muñoz-Goḿez et al., 2017;de Vries and Archibald, 2018). ...
Compared to nuclear genomes, mitochondrial genomes (mitogenomes) are small and usually code for only a few dozen genes. Still, identifying genes and their structure can be challenging and time-consuming. Even automated tools for mitochondrial genome annotation often require manual analysis and curation by skilled experts. The most difficult steps are (i) the structural modelling of intron-containing genes; (ii) the identification and delineation of Group I and II introns; and (iii) the identification of moderately conserved, non-coding RNA (ncRNA) genes specifying 5S rRNAs, tmRNAs and RNase P RNAs. Additional challenges arise through genetic code evolution which can redefine the translational identity of both start and stop codons, thus obscuring protein-coding genes. Further, RNA editing can render gene identification difficult, if not impossible, without additional RNA sequence data. Current automated mito- and plastid-genome annotators are limited as they are typically tailored to specific eukaryotic groups. The MFannot annotator we developed is unique in its applicability to a broad taxonomic scope, its accuracy in gene model inference, and its capabilities in intron identification and classification. The pipeline leverages curated profile Hidden Markov Models (HMMs), covariance (CMs) and ERPIN models to better capture evolutionarily conserved signatures in the primary sequence (HMMs and CMs) as well as secondary structure (CMs and ERPIN). Here we formally describe MFannot, which has been available as a web-accessible service (https://megasun.bch.umontreal.ca/apps/mfannot/) to the research community for nearly 16 years. Further, we report its performance on particularly intron-rich mitogenomes and describe ongoing and future developments.
... Classification of organisms has become exciting again, especially when common ground between the two eras is found. In some cases, the re-definition of a taxon may simply be enough (Barcytė et al., 2022), while in others, novel higher-rank taxa emerge and deserve formal recognition (Barcytė et al., 2021;Li et al., 2020;Muñoz-Gómez et al., 2017). This latter scenario is what applies to the the enigmatic red algal class Cyanidiophyceae revised recently by Park et al. (2023) and highlighted here. ...
... Red algae are at least a billion years old and have undergone significant remodeling, both with respect to their nuclear and organelle genomes 109 . The Rhodellophyceae contain the largest plastomes known 22 , whereas the Porphyridiophyceae contain expanded mitogenomes 23 . The Compsopogonophyceae have both large mitogenome and plastomes 18,21 . ...
Eukaryotic organelle genomes are generally of conserved size and gene content within phylogenetic groups. However, significant variation in genome structure may occur. Here, we report that the Stylonematophyceae red algae contain multipartite circular mitochondrial genomes (i.e., minicircles) which encode one or two genes bounded by a specific cassette and a conserved constant region. These minicircles are visualized using fluorescence microscope and scanning electron microscope, proving the circularity. Mitochondrial gene sets are reduced in these highly divergent mitogenomes. Newly generated chromosome-level nuclear genome assembly of Rhodosorus marinus reveals that most mitochondrial ribosomal subunit genes are transferred to the nuclear genome. Hetero-concatemers that resulted from recombination between minicircles and unique gene inventory that is responsible for mitochondrial genome stability may explain how the transition from typical mitochondrial genome to minicircles occurs. Our results offer inspiration on minicircular organelle genome formation and highlight an extreme case of mitochondrial gene inventory reduction.
... The high-throughput sequencing (HTS) made the acquisition of genomes more accessible, generating very large datasets at a reasonable cost . Phylogenomic studies based on organellar genomes have demonstrated its potential to elucidate relevant aspects of red algal evolution, providing support for phylogenies (Yang et al., 2015;Muñoz-Gómez et al., 2017;Nan et al., 2017) including those of difficult algal clades, which have been long-standing taxonomic conundrums, such as Rhodomelaceae (Díaz-Tapia et al., 2017) and Gracilariales Lyra et al., 2021). In this context, organellar genomes can generate robust and well-supported phylogenies at different taxonomic levels (Boo et al., 2016;Díaz-Tapia et al., 2017;Ng et al., 2017;Iha et al., 2018;Lyra et al., 2021). ...
Cystocloniacae is a highly diverse family of Rhodophyta, including species of ecological and economic importance, whose phylogeny remains largely unresolved. Species delimitation is unclear, particularly in the most speciose genus, Hypnea, and cryptic diversity has been revealed by recent molecular assessments, especially in the tropics. Here, we carried out the first phylogenomic investigation of Cystocloniaceae, focused on the genus Hypnea, inferred from chloroplast and mitochondrial genomes including taxa sampled from new and historical collections. In this work, molecular synapomorphies (gene losses, InDels and gene inversions) were identified to better characterize clades in our congruent organellar phylogenies. We also present taxon-rich phylogenies based on plastid and mitochondrial markers. Molecular and morphological comparisons of historic collections with contemporary specimens revealed the need for taxonomic updates in Hypnea, the synonymization of H. marchantae to a later heterotypic synonym of H. cervicornis and the description of three new species: H. davisiana sp. nov., H. djamilae sp. nov. and H. evaristoae sp. nov.
... The nuclear and plastid genomes of the ancestral archaeplastid were large and gene-rich [52] compared to the small genomes of rhodophytes, suggesting large-scale genome reduction with the early origin of red algae [24,53,54]. Subsequently, two cycles of genome reduction Box 1. Major groups of Archaeplastida Archaeplastida is a highly diverse group that comprises an estimated 450 000-500 000 species (see Figure 1 in main text) [151][152][153][154]. ...
Plant (archaeplastid) evolution has transformed the biosphere, but we are only now beginning to learn how this took place through comparative genomics, phylogenetics, and the fossil record. This has illuminated the phylogeny of Archaeplastida, Viridiplantae, and Streptophyta, and has resolved the evolution of key characters, genes, and genomes – revealing that many key innovations evolved long before the clades with which they have been casually associated. Molecular clock analyses estimate that Streptophyta and Viridiplantae emerged in the late Mesoproterozoic to late Neoproterozoic, whereas Archaeplastida emerged in the late-mid Palaeoproterozoic. Together, these insights inform on the coevolution of plants and the Earth system that transformed ecology and global biogeochemical cycles, increased weathering, and precipitated snowball Earth events, during which they would have been key to oxygen production and net primary productivity (NPP).
... Also shown is whether respective groups are unicellular or multicellular organisms and whether sexual reproduction has been observed. The topologies in red algae (Rhodophyta) (66,67) and Viridiplantae (4) are based on previous studies. The order of branching of red algae and Glaucophyta remains unclear, although a recent study based on large-scale genomic data suggests that red algae branched first in Archaeplastida (4). ...
Sexual reproduction is widespread in eukaryotes; however, only asexual reproduction has been observed in unicellular red algae, including Galdieria , which branched early in Archaeplastida. Galdieria possesses a small genome; it is polyextremophile, grows either photoautotrophically, mixotrophically, or heterotrophically, and is being developed as an industrial source of vitamins and pigments because of its high biomass productivity. Here, we show that Galdieria exhibits a sexual life cycle, alternating between cell-walled diploid and cell wall–less haploid, and that both phases can proliferate asexually. The haploid can move over surfaces and undergo self-diploidization or generate heterozygous diploids through mating. Further, we prepared the whole genome and a comparative transcriptome dataset between the diploid and haploid and developed genetic tools for the stable gene expression, gene disruption, and selectable marker recycling system using the cell wall–less haploid. The BELL/KNOX and MADS-box transcription factors, which function in haploid-to-diploid transition and development in plants, are specifically expressed in the haploid and diploid, respectively, and are involved in the haploid-to-diploid transition in Galdieria , providing information on the missing link of the sexual life cycle evolution in Archaeplastida. Four actin genes are differently involved in motility of the haploid and cytokinesis in the diploid, both of which are myosin independent and likely reflect ancestral roles of actin. We have also generated photosynthesis-deficient mutants, such as blue-colored cells, which were depleted in chlorophyll and carotenoids, for industrial pigment production. These features of Galdieria facilitate the understanding of the evolution of algae and plants and the industrial use of microalgae.
... Red algal systematics have been improved to reflect the reconstructed evolutionary histories based on molecular phylogenetic analysis (Saunders and Hommersand 2004;Yoon et al. 2006Yoon et al. , 2010Muñoz-Gómez et al. 2017 This genus includes 20 described species with two infraspecific taxa to date (Fig. 2;Kikuchi and Niwa 2020;Guiry and Guiry 2021). Among the currently accepted names, however, N. pulchella and Pyropia stamfordensis are regarded as heterotypic synonyms of N. kuniedae based on their identical sequences of rbcL (Kim et al. 2018b; see Table 1), and four undescribed species were counted in the molecular phylogenetic tree see Fig. 6). ...
Neopyropia J. Brodie & L.-E Yang has been cultivated in Asia for centuries and the total production was nearly three million (fresh weight) with an economic value of US$2.7 billion in 2019. It has been traditionally used as human food. Recently its diverse secondary metabolites as functional components, including porphyrin, phycobiliproteins, carotenoids, mycosporine-like amino acids (MAAs) in the cosmetic and pharmaceutical industries have received much attention. In this review we first discuss the nomenclatural history of Neopyropia, its characterization, and circumscription and species delineation; current systematics, biogeography and speciation, genomics and transcriptomics, ecology, life history, cultivation, and bioactive chemicals. Currently, 22 species have been described in this genus and 32 varieties or cultivars have been developed in Korea, China, and Japan. Most species show a large degree of phenotypic plasticity. This genus may be found on all continents except for the Antarctic. Neopyropia has a heteromorphic life cycle, alternating macroscopic foliose monoecious gametophytic phase and a filamentous sporophytic phase, called the conchocelis. The gametophytic thallus consists of one cell layers in thickness with an extremely high surface area to volume ratio, and therefore, all cells can take up nutrients. Neopyropia can be found in various environments: from marine to estuarine; from eulittoral to sublittoral; and may be epilithic, epiphytic or epizoic. Neopyropia yezoensis has received much more attention than other species in this genus because this species is the dominant aquaculture species and has rapid growth. Recently, a complete plastid and mitochondria genome has been described in N. yezoensis, which provides critical insights to understand the origin and evolution of eukaryotes and the evolution of agronomic traits. This review will describe the most recent advances in these areas.
... We assembled the transcriptome de novo in this study for the remaining 79 species. To make the species phylogenetic tree displayed on the left side of Figure 2, the evolutionary relationships among clades were taken from Burki et al. 2020 [36] and the within-clade phylogenies were taken from the following papers: Alveolata [90], Amoebozoa [91], Centrohelida, Cryptista and Haptophyta [41], Chlorophyta [92,93], Discoba [94], fungi [95][96][97], Holozoa [95,98,99], Metamonada [100], Rhizaria [101,102], Stramenopiles [103] and Rhodophyta [104]. ...
Two autophagy-related (ATG) ubiquitin-like conjugation systems, the ATG12 and ATG8 systems, play important roles in macroautophagy. While multiple duplications and losses of the ATG conjugation system proteins are found in different lineages, the extent to which the underlying systems diversified across eukaryotes is not fully understood. Here, in order to understand the evolution of the ATG conjugation systems, we constructed a transcriptome database consisting of 94 eukaryotic species covering major eukaryotic clades and systematically identified ATG conjugation system components. Both ATG10 and the C-terminal glycine of ATG12 are essential for the canonical ubiquitin-like conjugation of ATG12 and ATG5. However, loss of ATG10 or the C-terminal glycine of ATG12 occurred at least 16 times in a wide range of lineages, suggesting that possible covalent-to-non-covalent transition is not limited to the species that we previously reported such as Alveolata and some yeast species. Some species have only the ATG8 system (with conjugation enzymes) or only ATG8 (without conjugation enzymes). More than 10 species have ATG8 homologs without the conserved C-terminal glycine, and Tetrahymena has an ATG8 homolog with a predicted transmembrane domain, which may be able to anchor to the membrane independent of the ATG conjugation systems. We discuss the possibility that the ancestor of the ATG12 and ATG8 systems is more similar to ATG8. Overall, our study offers a whole picture of the evolution and diversity of the ATG conjugation systems among eukaryotes, and provides evidence that functional diversifications of the systems are more common than previously thought. Abbreviations: APEAR: ATG8–PE association region; ATG: autophagy-related; LIR: LC3-interacting region; NEDD8: neural precursor cell expressed, developmentally down-regulated gene 8; PE: phosphatidylethanolamine; SAMP: small archaeal modifier protein; SAR: Stramenopiles, Alveolata, and Rhizaria; SMC: structural maintenance of chromosomes; SUMO: small ubiquitin like modifier; TACK: Thaumarchaeota, Aigarchaeota, Crenarchaeota, and Korarchaeota; UBA: ubiquitin like modifier activating enzyme; UFM: ubiquitin fold modifier; URM: ubiquitin related modifier.
... Among these six classes, only the 3 latter contain microalgae, single-celled or mesophilic pseudofilamentous. More recently, this classification has been revised again on basis of plastid genomes sequences [5]. For these authors, the cyanidiophytina is a subphylum of Rhodophyta and the former rhodophytina subphylum has been splitted into 2 different subphylum named proteorhodophytina (containing Compsopogonophyceae, Porphyridiophyceae, Rhodellophyceae and Stylonematophyceae) and Eurhodophytina (Bangiophyceae and Florideophyceae classes). ...
Microalgae constitute a remarkable biological diversity but a limited number of them have been the object of study for their ability to produce exoplysaccharides (EPS). Among them, the red marine microalgae Porphyridium or Rhodella produce sulphated EPS, exhibiting some biological activities with potential interest in the pharmaceutical and cosmetic industries. EPS from Porphyridium and Rhodella being relatively similar in their composition, it has long been considered that all the red microalgae produced similar EPS and no attention was paid to other red microalgae. The objective of our work was then to explore the diversity of red microalgae for the production of EPS, focusing in this first step on the screening of the strains for their ability to produce EPS and preliminary structural characterization. The study was conducted with 11 microalgae strains belonging to the proteorhodophytina subphylum. All microalgae were able to produce EPS, released in the culture medium (strains belonging to Porphyridiophyceae and Rhodellophyceae classes) or remaining bound to the cells (strains from Stylonematophyceae class). The analysis of monosaccharides composition was found significantly different, with for instance high levels of glucuronic acids in the EPS from C. japonica and N. cyanea, but also strong differences in the sulphation degrees of polymers (between 1.2 and 28.7% eq. SO4).
... As noted by [10], 98% of plastomes are under 200 kbp and harbour modest amounts (< 50%) of non-coding DNA. The L. pallida plastome, reaching 362.3 kbp, may not seem that impressive in comparison with the giant plastomes recently reported from some photosynthetic species, including the distantly related chlamydomonadalean Haematococcus lacustris (1.35 Mbp; [9]) or certain red algae (up to 1.13 Mbp; [57]); however, it by far dwarfs the plastomes of all non-photosynthetic eukaryotes studied to date. The previous record holder, the ~230 kbp plastome of Polytoma uvella [8], is only two thirds of the size of the L. pallida plastome. ...
Background
The plastid genomes of the green algal order Chlamydomonadales tend to expand their non-coding regions, but this phenomenon is poorly understood. Here we shed new light on organellar genome evolution in Chlamydomonadales by studying a previously unknown non-photosynthetic lineage. We established cultures of two new Polytoma-like flagellates, defined their basic characteristics and phylogenetic position, and obtained complete organellar genome sequences and a transcriptome assembly for one of them.
Results
We discovered a novel deeply diverged chlamydomonadalean lineage that has no close photosynthetic relatives and represents an independent case of photosynthesis loss. To accommodate these organisms, we establish the new genus Leontynka, with two species (L. pallida and L. elongata) distinguishable through both their morphological and molecular characteristics. Notable features of the colourless plastid of L. pallida deduced from the plastid genome (plastome) sequence and transcriptome assembly include the retention of ATP synthase, thylakoid-associated proteins, the carotenoid biosynthesis pathway, and a plastoquinone-based electron transport chain, the latter two modules having an obvious functional link to the eyespot present in Leontynka. Most strikingly, the ~362 kbp plastome of L. pallida is by far the largest among the non-photosynthetic eukaryotes investigated to date due to an extreme proliferation of sequence repeats. These repeats are also present in coding sequences, with one repeat type found in the exons of 11 out of 34 protein-coding genes, with up to 36 copies per gene, thus affecting the encoded proteins. The mitochondrial genome of L. pallida is likewise exceptionally large, with its >104 kbp surpassed only by the mitogenome of Haematococcus lacustris among all members of Chlamydomonadales hitherto studied. It is also bloated with repeats, though entirely different from those in the L. pallida plastome, which contrasts with the situation in H. lacustris where both the organellar genomes have accumulated related repeats. Furthermore, the L. pallida mitogenome exhibits an extremely high GC content in both coding and non-coding regions and, strikingly, a high number of predicted G-quadruplexes.
Conclusions
With its unprecedented combination of plastid and mitochondrial genome characteristics, Leontynka pushes the frontiers of organellar genome diversity and is an interesting model for studying organellar genome evolution.
... Muñoz-Gómez, Mejía-Franco, Durnin, Colp, Grisdale, J.M. Archibald et Slamovits 2017: e3. Note: The new subphylum joins two other subphyla of red algae, the Cyanidiophytina and Eurhodophytina, and contains the classes Compsopogonophyceae, Porphyridiophyceae, Rhodellophyceae and Stylonematophyceae Muñoz-Gómez et al. 2017 (Yang et al. 2020) but is sometimes nested within Neopyropia (e.g., Kucera and Saunders 2012;Mateo-Cid et al. 2012). Phylogenetic analyses using plastid and/or mitochondrial genomes may be able to better resolve the position of Porphyrella (Yang et al. 2020 ...
The fifth addendum to Schneider and Wynne’s 2007 “A synoptic review of the classification of red algal genera a half century after Kylin’s 1956 ‘ Die Gattungen der Rhodophyceen ’” is presented, covering the names of genus- and higher-level taxa added or modified since our fourth addendum ( Bot. Mar. 62: 355–367). Since the original compilation, we have added 21 new genera in the first addendum, 27 in the second, 40 in the third and 58 in the fourth, demonstrating the increasing amount of genetic work over more than a decade. In this fifth addendum, we add 31 new genera, three new families, two new orders, and one new subphylum from the past three years, as well as listing four genera reinstated from synonymy based upon molecular sequencing studies.
... Cryptophytes, dinoflagellates, diatoms, haptophytes have absorbed red algae (Keeling, 2010;Ponce-Toledo et al., 2019). Some might even have arisen after tertiary endosymbiosis, as the secondary red plastids appear to be monophyletic (Munoz-Gomez et al., 2017) but their hosts are not. Their origins are for some still quite hotly debated. ...
Following endosymbiosis, the chloroplast genome shrunk and became reliant on the host genome for its expression. In Chlamydomonas reinhardtii, Octotricopeptide repeat proteins (OPR), encoded in the nucleus, control the expression of a specific organellar mRNA. The OPR repeat is a degenerate motif of 38 amino-acids, folding into a tandem of antiparallel α-helices which can bind to RNA. An individual OPR repeat is predicted to interact with one given nucleotide thanks to specificity-conferring residues at defined positions within the repeat. OPR proteins contain tracks of successive OPR motifs, thus they can bind to a specific RNA “target” sequence and act on it. I aimed to study this specificity, called the “OPR code”, starting with a draft code based on known OPR protein/mRNA couples. I mutated in vivo the chloroplast targets of some OPR factors to disrupt the OPR/RNA interaction, and then tried to restore it by mutating the specificity-conferring residues in the corresponding repeats. Surprisingly, OPR/RNA interactions seem very resilient, challenging our view of how the specificity is established in vivo. Complementary functional studies that I performed on the OPR factors MDB1 and MTHI1 revealed that chloroplast gene expression might rely on complex networks of nuclear factors. By cooperating those putative systems would be both more specific and more resilient.
... Los organismos fotosintéticos han desarrollado varios sistemas de captura de la radiación para asegurar una eficiente transferencia energética y P. purpureum tiene estrategias en su maquinaria fotosintética con ficobilisomas (complejos de ficobiliproteinas) y proteínas del complejo de fotopigmentos (clorofila, carotenoides) que estabilizan sus funciones y favorecen su adaptación como se presenta en las células rojizas (ficoeritrina) de los humedales costeros. El genoma de P. purpureum ha demostrado una diversidad de historias evolutivas con origen genético de procariontes y eucariontes que ha enriquecido el árbol fotosintético de la vida (Bhattacharya et al., 2013;Muñoz-Gómez et al., 2017). ...
Las lagunas costeras tropicales, superficiales están localizadas en la Costa Central del Pacífico en Sudamérica. Colecciones cianobacterial y microalgal estándar del humedal de Puerto Viejo (Laguna Grande, lado norte del humedal), departamento de Lima, fueron realizadas con registros irregulares de parámetros físico- químicos entre 2005 y 2010. Poblaciones naturales planctónicas de Rhabdoderma lineare Schmidle et Lauterborn en verano y otoño, exhibieron variaciones morfológicas celulares y coloniales. R. lineare formó floraciones asociadacon la rodofita unicelular Porphyridium purpureum (Bory) Drew & Rossen condiciones eutróficas y salinas, con rango de temperatura entre 25 – 33 ºC, gradiente de salinidad de 13 - 20 ppt (NaCl) y rango de pH 8 a 9. La plasticidad fenotípica de las especies y sus patrones distribucionales (planctónica y bentónica) en laguna somera están relacionadas con sus estrategias de vida que favorecen la colonización exitosa en lagunas costeros expuestos a régimen hídrico anual con periodos de inundación y desecación. Rhabdoderma lineare y Porphyridium purpureum son nuevos registros para la flora Peruana.
... Red algae (Rhodophyta) are divided into 3 subphyla [6] (Figure 1c) that have great morphological and ecological variation. One subphylum (Cyanidiophytina) contains unicellular extremophiles that are acidophilic and/or thermophilic. ...
The cytoskeleton has a central role in eukaryotic biology, enabling cells to organize internally, polarize, and translocate. Studying cytoskeletal machinery across the tree of life can identify common elements, illuminate fundamental mechanisms, and provide insight into processes specific to less‐characterized organisms. Red algae represent an ancient lineage that is diverse, ecologically significant, and biomedically relevant. Recent genomic analysis shows that red algae have a surprising paucity of cytoskeletal elements, particularly molecular motors. Here, we review the genomic and cell biological evidence and propose testable models of how red algal cells might perform processes including cell motility, cytokinesis, intracellular transport, and secretion, given their reduced cytoskeletons. In addition to enhancing understanding of red algae and lineages that evolved from red algal endosymbioses (e.g., apicomplexan parasites), these ideas may also provide insight into cytoskeletal processes in animal cells. Many red algae are capable of motility and furrowing cytokinesis despite their reduced cytoskeletal toolbox relative to animals and amoebae. Flagella are not present in any red alga, and most characterized members of this ancient eukaryotic group lack both myosin and Arp2/3.
... The plastid-encoded protein sequences obtained by in silico translation (Expasy; https://web.expasy.org/ translate/) were added to the single protein datasets used in Muñ oz-Gó mez et al. 55 Some redundant taxa in the red algae were removed prior to further analysis. Alignment and removal of ambiguously aligned positions were performed as described above, except that the Gblocks option was set to t = p. ...
Rapidly accumulating genetic data from environmental sequencing approaches have revealed an extraordinary level of unsuspected diversity within marine phytoplankton,1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11 which is responsible for around 50% of global net primary production.¹²,¹³ However, the phenotypic identity of many of the organisms distinguished by environmental DNA sequences remains unclear. The rappemonads represent a plastid-bearing protistan lineage that to date has only been identified by environmental plastid 16S rRNA sequences.14, 15, 16, 17 The phenotypic identity of this group, which does not confidently cluster in any known algal clades in 16S rRNA phylogenetic reconstructions,¹⁵ has remained unknown since the first report of environmental sequences over two decades ago. We show that rappemonads are closely related to a haptophyte microalga, Pavlomulina ranunculiformis gen. nov. et sp. nov., and belong to a new haptophyte class, the Rappephyceae. Organellar phylogenomic analyses provide strong evidence for the inclusion of this lineage within the Haptophyta as a sister group to the Prymnesiophyceae. Members of this new class have a cosmopolitan distribution in coastal and oceanic regions. The relative read abundance of Rappephyceae in a large environmental barcoding dataset was comparable to, or greater than, those of major haptophyte species, such as the bloom-forming Gephyrocapsa huxleyi and Prymnesium parvum, and this result indicates that they likely have a significant impact as primary producers. Detailed characterization of Pavlomulina allowed for reconstruction of the ancient evolutionary history of the Haptophyta, a group that is one of the most important components of extant marine phytoplankton communities.
... Smith (2020) indicated that panlindromic repeats are mutational hotspots, and contribute to plastome expansion in chlamydomonadalean Chlorosarcinopsis eremi. In addition to this study, the proliferation of non-coding regions was mainly documented in algae (Muñoz-Gómez et al., 2017;Gaouda et al., 2018;Smith, 2018), and the non-coding DNA of Haematococcus lacustris comprises over 90% of the plastome (Smith, 2018). In addition, we also found high AT regions in Paphiopedilum (trnS-trnG, trnE-trnT, and trnP-psaJ) (unpublished data). ...
The size of the chloroplast genome (plastome) of autotrophic angiosperms is generally conserved. However, the chloroplast genomes of some lineages are greatly expanded, which may render assembling these genomes from short read sequencing data more challenging. Here, we present the sequencing, assembly, and annotation of the chloroplast genomes of Cypripedium tibeticum and Cypripedium subtropicum. We de novo assembled the chloroplast genomes of the two species with a combination of short-read Illumina data and long-read PacBio data. The plastomes of the two species are characterized by expanded genome size, proliferated AT-rich repeat sequences, low GC content and gene density, as well as low substitution rates of the coding genes. The plastomes of C. tibeticum (197,815 bp) and C. subtropicum (212,668 bp) are substantially larger than those of the three species sequenced in previous studies. The plastome of C. subtropicum is the longest one of Orchidaceae to date. Despite the increase in genome size, the gene order and gene number of the plastomes are conserved, with the exception of an ∼75 kb large inversion in the large single copy (LSC) region shared by the two species. The most striking is the record-setting low GC content in C. subtropicum (28.2%). Moreover, the plastome expansion of the two species is strongly correlated with the proliferation of AT-biased non-coding regions: the non-coding content of C. subtropicum is in excess of 57%. The genus provides a typical example of plastome expansion induced by the expansion of non-coding regions. Considering the pros and cons of different sequencing technologies, we recommend hybrid assembly based on long and short reads applied to the sequencing of plastomes with AT-biased base composition.
... The basal position of Cyanidiales is without doubt, which is then followed by two smaller clades. I retained the conventional notion that Stylonematales is sister to Compsopogonales, although another study including fewer taxa (Muñoz-Gómez et al., 2017) has placed this group as sister to Rhodellophyceae. Both surveys confirm that an overwhelming majority of rhodophytes belong to the monophyletic Eurhodophytina (Bangiales plus Florideophyceae). ...
The present article has two primary objectives. First, the article provides a historical overview of graphical tools used in the past centuries for summarizing the classification and phylogeny of plants. It is emphasized that each published diagram focuses on only a single or a few aspects of the present and past of plant life on Earth. Therefore, these diagrams are less useful for communicating general knowledge in botanical research and education. Second, the article offers a solution by describing the principles and methods of constructing a lesser- known image type, the coral, whose potential usefulness in phylogenetics was first raised by Charles Darwin. Cladogram topology, phylogenetic classification and nomenclature, diversity of taxonomic groups, geological timescale, paleontological records, and other relevant information on the evolution of Archaeplastida are simultaneously condensed for the first time into the same figure – the Coral of Plants. This image is shown in two differently scaled parts to efficiently visualize as many details as possible, because the evolutionary timescale is much longer, and the extant diversity is much lower for red and green algae than for embryophytes. A fundamental property of coral diagrams, that is their self-similarity, allows for the redrawing of any part of the diagram at smaller scales.
... The precise nature of the algal donor is similarly unclear. At present, the data suggest that red alga-type complex plastids share more recent common ancestry with those of mesophilic red algae such as Porphyra and Chondrus than they do with the plastids of extremophiles such as Cyanidioschyzon and Galdieria (e.g., Sev c ıkov a et al. 2015; Kim et al. 2017;Muñoz-G omez et al. 2017). ...
The origin of plastids (chloroplasts) by endosymbiosis stands as one of the most important events in the history of eukaryotic life. The genetic, biochemical, and cell biological integration of a cyanobacterial endosymbiont into a heterotrophic host eukaryote more than a billion years ago paved the way for the evolution of diverse algal groups in a wide range of aquatic and, eventually, terrestrial environments. Plastids have on multiple occasions also moved horizontally from eukaryote to eukaryote by secondary and tertiary endosymbiotic events. The overall picture of extant photosynthetic diversity can best be described as 'patchy': plastid-bearing lineages are spread far and wide across the eukaryotic tree of life, nested within heterotrophic groups. The algae do not constitute a monophyletic entity and understanding how, and how often, plastids have moved from branch to branch on the eukaryotic tree remains one of the most fundamental unsolved problems in the field of cell evolution. In this review we provide an overview of recent advances in our understanding of the origin and spread of plastids from the perspective of comparative genomics. Recent years have seen significant improvements in genomic sampling from photosynthetic and non-photosynthetic lineages, both of which have provided important pieces to add to the puzzle of plastid evolution. Comparative genomics has also allowed us to better understand how endosymbionts become organelles.
... In this regard, the genomic data of both nuclei and nucleomorphs, as well as transcriptomic and proteomic data, have been accumulated for cryptophytes and chlorarachniophytes (13)(14)(15)(16)(17)(18)(19)(20)(21)(22), and genetic transformation was established for a chlorarachniophyte species (23). It has been determined that a red alga and an ulvophyte green alga are the sources of cryptophyte and chlorarachniophyte plastids, respectively (18,(24)(25)(26)(27)(28), but an even recent multigene phylogenetic analyses did not provide finer resolution in determining the closest living species/genus for the origins of the two plastids (18,(28)(29)(30)(31)(32). Such uncertainties are potential drawbacks of using cryptophytes and chlorarachniophytes as the model organisms to study the effect of the reductive process on the endosymbiont genome during secondary endosymbiosis. ...
Nucleomorphs are relic endosymbiont nuclei so far found only in two algal groups, cryptophytes and chlorarachniophytes, which have been studied to model the evolutionary process of integrating an endosymbiont alga into a host-governed plastid (organellogenesis). However, past studies suggest that DNA transfer from the endosymbiont to host nuclei had already ceased in both cryptophytes and chlorarachniophytes, implying that the organellogenesis at the genetic level has been completed in the two systems. Moreover, we have yet to pinpoint the closest free-living relative of the endosymbiotic alga engulfed by the ancestral chlorarachniophyte or cryptophyte, making it difficult to infer how organellogenesis altered the endosymbiont genome. To counter the above issues, we need novel nucleomorph-bearing algae, in which endosymbiont-to-host DNA transfer is on-going and for which endosymbiont/plastid origins can be inferred at a fine taxonomic scale. Here, we report two previously undescribed dinoflagellates, strains MGD and TGD, with green algal endosymbionts enclosing plastids as well as relic nuclei (nucleomorphs). We provide evidence for the presence of DNA in the two nucleomorphs and the transfer of endosymbiont genes to the host (dinoflagellate) genomes. Furthermore, DNA transfer between the host and endosymbiont nuclei was found to be in progress in both the MGD and TGD systems. Phylogenetic analyses successfully resolved the origins of the endosymbionts at the genus level. With the combined evidence, we conclude that the host–endosymbiont integration in MGD/TGD is less advanced than that in cryptophytes/chrorarachniophytes, and propose the two dinoflagellates as models for elucidating organellogenesis.
... We first constructed a consensus eukaryotic species tree based on recent bibliographical references (James et al. 2006;Dunn et al. 2014;Ruhfel et al. 2014;Kurtzman et al. 2015;Lowe et al. 2015;Derelle et al. 2016;He et al. 2016;Qiu et al. 2016;Sierra et al. 2016;McCarthy and Fitzpatrick 2017;Munoz-Gomez et al. 2017;Simion et al. 2017;Torruella et al. 2018). We generated one tree per subunit family (ORC2, ORC3, ORC4, and ORC5; CDC6 and ORC1 in the same tree). ...
The conservation of orthologs of most subunits of the origin recognition complex (ORC) has served to propose that the whole complex is common to all eukaryotes. However, various uncertainties have arisen concerning ORC subunit composition in a variety of lineages. Also, it is unclear whether the ancestral diversification of ORC in eukaryotes was accompanied by the neofunctionalization of some subunits, e.g., role of ORC1 in centriole homeostasis. We have addressed these questions by reconstructing the distribution and evolutionary history of ORC1-5/CDC6 in a taxon-rich eukaryotic dataset. First, we identified ORC subunits previously undetected in divergent lineages, which allowed us to propose a series of parsimonious scenarios for the origin of this multiprotein complex. Contrary to previous expectations, we found a global tendency in eukaryotes to increase or decrease the number of subunits as a consequence of genome duplications or streamlining, respectively. Interestingly, parasites show significantly lower number of subunits than free-living eukaryotes, especially those with the lowest genome size and gene content metrics. We also investigated the evolutionary origin of the ORC1 role in centriole homeostasis mediated by the PACT region in human cells. In particular, we tested the consequences of reducing ORC1 levels in the centriole-containing green alga Chlamydomonas reinhardtii. We found that the proportion of centrioles to flagella and nuclei was not dramatically affected. This, together with the PACT region not being significantly more conserved in centriole-bearing eukaryotes, support the notion that this neofunctionalization of ORC1 would be a recent acquisition rather than an ancestral eukaryotic feature.
Ochrophyta is a vast and morphologically diverse group of algae with complex plastids, including familiar taxa with fundamental ecological importance (diatoms or kelp), and a wealth of lesser-known and obscure organisms. The sheer diversity of ochrophytes poses a challenge for reconstructing their phylogeny, with major gaps in sampling and an unsettled placement of particular taxa yet to be tackled. We sequenced transcriptomes from 25 strategically selected representatives and used these data to build the most taxonomically comprehensive ochrophyte-centered phylogenomic supermatrix to date. We employed a combination of approaches to reconstruct and critically evaluate the relationships among ochrophytes. While generally congruent with previous analyses, the updated ochrophyte phylogenomic tree resolved the position of several taxa with previously uncertain placement, and supported a redefinition of the class Synchromophyceae. Our results indicated that the heterotrophic plastid-lacking heliozoan Actinophrys sol is not a sister lineage of ochrophytes, as proposed recently, but rather phylogenetically nested among them. In addition, we found Picophagus flagellatus to be a secondarily heterotrophic ochrophyte lacking all hallmark plastid genes, yet exhibiting mitochondrial proteins that seem to be genetic footprints of lost plastid organelle. We thus document, for the first time, plastid loss in two separate ochrophyte lineages. Altogether, our study provides a new framework for reconstructing trait evolution in ochrophytes and demonstrates that plastid loss is more common than previously thought.
Issue Section: Discoveries
Hypothetical chloroplast open reading frames (ycfs) are putative genes in the plastid genomes of photosynthetic eukaryotes. Many ycfs are also conserved in the genomes of cyanobacteria, the presumptive ancestors of present-day chloroplasts. The functions of many ycfs are still unknown. Here, we generated knock-out mutants for ycf51 (sll1702) in the cyanobacterium Synechocystis sp. PCC 6803. The mutants showed reduced photoautotrophic growth due to impaired electron transport between photosystem II (PSII) and PSI. This phenotype results from greatly reduced PSI content in the ycf51 mutant. The ycf51 disruption had little effect on the transcription of genes encoding photosynthetic complex components and the stabilization of the PSI complex. In vitro and in vivo analyses demonstrated that Ycf51 cooperates with PSI assembly factor Ycf3 to mediate PSI assembly. Furthermore, Ycf51 interacts with the PSI subunit PsaC. Together with its specific localization in the thylakoid membrane and the stromal exposure of its hydrophilic region, our data suggest that Ycf51 is involved in PSI complex assembly. Ycf51 is conserved in all sequenced cyanobacteria, including the earliest branching cyanobacteria of the Gloeobacter genus, and is also present in the plastid genomes of glaucophytes. However, Ycf51 has been lost from other photosynthetic eukaryotic lineages. Thus, Ycf51 is a PSI assembly factor that has been functionally replaced during the evolution of oxygenic photosynthetic eukaryotes.
Thalli of the endemic epiphytic New Zealand red seaweed Pyrophyllon subtumens are known to contain a high level of xylose and a notable amount of arabinose but the extracted polysaccharide has not been characterised. The linkage/substitution of individual sugars within the water-soluble polysaccharide extract and various derivatives were determined by chemical and spectroscopic methods. No 3-linked sugars nor any d-galactose were found, which excluded agar-, carrageenan- or mixed 3-linked/4-linked β-d-xylan-type polysaccharides found in many other red macroalgae. Instead, the polysaccharide backbone contained predominantly 4-linked β-d-xylopyranosyl, 4-linked 3,6-anhydro-l-galactopyranosyl and 4-linked l-galactopyranosyl units. Some of each type of sugar were sulfated at various positions. Some xylosyl units were substituted at the 2- or 3-position with l-arabinosyl units. The polysaccharide is complex and likely contains a range of structures. However, partial sequencing was successfully used to recover and identify a novel disaccharide 4-O-d-xylopyranosyl-3,6-anhdydro-l-galactopyranose, which indicates a unique →4)-β-d-Xylp-(1 → 4)-3,6-anhydro-l-Galp-(1 → repeat unit in the polysaccharide.
The monograph is devoted to a review of the higher taxa of eu-karyotes and the approaches to the problem of their rank correlation. Significant milestones in the history of eukaryotic megasys-tematics are touched upon. The principles and approaches to the nomenclature of the higher taxa of eukaryotes are discussed. A revision of the system of eukaryotic organisms was carried out with re-ference to the original descriptions. The tendencies of general system transformation are considered and problems with some practical applications of eukaryotic megasystematics are discussed. The Obimoda subdomain, the Crumalia kingdom, the Mantamonadea, Rigifilidea, and Collodictyonidea phyla are described. A retrospective overview of basic systems of eukaryotes published in the period 1925—2022 and an extensive list of publications on megasystematics and microbiology of eukaryotes are presented.
Tags: protozoans, algae, eukaryotes, megasystematics, taxon rank, eukaryotic supergroups, Cavalier-Smith, Ehrenberg, Opimoda, Loukozoa, Amoebozoa, Opisthokonta, Discoba, Euglenozoa, Archaeplastida, Cryptista, Haptista, Chromalveolata, Heterokonta, Provora, Telonemia, Oomycetes, Fungi, Florideae hypothesis
Les mitochondries et les chloroplastes sont des organites de cellules eucaryotes issus d’événements endosymbiotiques impliquant une bactérie et une cellule hôte il y a plus d’un milliard d’années. Aujourd’hui la très grande majorité des protéines présentes dans ces organites sont codées dans le noyau. Le ciblage des protéines cytosoliques vers les mitochondries et les chloroplastes pourrait dériver d’un mécanisme de résistance bactérienne aux attaques de peptides antimicrobiens, ces acteurs majeurs de l’immunité innée, présents dans tous les domaines du vivant. Cette hypothèse se base sur les similarités frappantes entre ces deux mécanismes. Au cours de mon doctorat, j’ai mis à l’épreuve cette hypothèse. Dans une première partie, j’ai pu montrer qu’un sous-ensemble de peptides antimicrobiens se structurant en hélice ↵-amphipathique et les peptides d’adressage possédaient des propriétés physico-chimiques communes, qui sont distinctes de celles partagées entre les peptides signaux de sécrétion bactériens et eucaryotes dont l’origine évolutive commune est bien établie. De plus, ils peuvent se complémenter fonctionnellement in vivo, confortant l’hypothèse de leur origine commune (Garrido et al. 2020). La transition moléculaire nécessaire pour passer d’un peptide antimicrobien à un peptide d’adressage comporte trois étapes cruciales : i) le remplacement des lysines par des arginines qui permet de diminuer l’activité microbienne et de favoriser l’activité d’adressage, ii) l’acquisition d’un site de clivage au sein des peptides d’adressage, iii) l’acquisition d’un domaine N-terminal peu structuré afin d’orienter l’adressage vers le chloroplaste et non vers la mitochondrie au sein des eucaryotes photosynthétiques (Caspari, Garrido et al., article soumis). Dans une deuxième partie, j’ai établi le catalogue exhaustif des familles d’homologues des peptidases impliquées dans la dégradation des peptides d’adressage dans l’arbre du vivant. J’ai pu démontrer que chacune de ces peptidases a été acquise via un évènement de transfert horizontal depuis une bactérie. En accord avec notre hypothèse, on retrouve de nombreux homologues de bactéries résistantes aux peptides antimicrobiens proches des peptidases des organites (Garrido et al., article soumis).
The trend in naming genera based almost exclusively on molecular data, and not on morphological diagnostic characters, is increasing. In bifurcating phylogenetic trees generic cut-offs are arbitrary, but at the bare minimum nomenclatural changes should be supported by multiple phylogenetic methodologies using appropriate models for all the various gene partitions, strong support with all branch support methods, and should also result in adding to our knowledge of the interrelationships of taxa. We believe that a recent taxonomic treatment of the genus Pyropia (Yang et al. 2020) into several genera is unwarranted. We reanalysed the data presented in the recent article, using additional phylogenetic methods. Our results show that many of the newly established genera are not well supported by all methods, and the new circumscription of the genus Pyropia renders it unsupported. We also tested additional outgroups, which were previously suggested as sister to Pyropia, but this did not substantially change our conclusions. These generic nomenclatural changes of the previously strongly supported genus Pyropia, do not shed light on the evolution of this group and have serious consequences in these commercially important algae, that are also governed by a plethora of regulation and by-laws that now need to be amended. We suggest that the over-splitting of groups based only on poorly produced and modestly supported phylogenies should not be accepted and that the genus Pyropia sensu Sutherland et al. (2011) be restored.
Grateloupia gibbesii Harvey (family; Halymeniaceae) is a newly recorded red alga in the Egyptian Mediterranean Sea. In the present study, Grateloupia gibbesii polysaccharide was isolated by hot aqueous extraction and then precipitated by cold ethanol. The yield of crude polysaccharides was 6.4% (w/w), which increased to 17% (w/w) after deproteinization. Preliminary structural characterization and bioactivity of the deproteinized polysaccharide (DGP) were investigated. The monosaccharides' contents were identified by TLC and HPLC. Preliminary structural estimation was carried out by FT-IR and ¹H NMR. Moreover, in-vitro exploration of anticoagulant activity by prothrombin time (PT) and fibrinolytic activity of the polysaccharide was determined. The antioxidant activity was determined by the 2,2-diphenyl-1-picrylhydrazyl (DPPH) assay, and the prebiotic activity was assessed against Lactobacillus spp. bacteria. The molecular weight of DGP was 286 kDa and galactose was the most abundant monomer with traces of xylose and glucuronic acid. Anticoagulant tests of DGP revealed prolonged clotting and prothrombin times (20 &14 s at a concentration of 2 mg/mL), respectively, showing moderate anticoagulant activity. DGP exhibited significant fibrinolytic activity (50%), relatively high antioxidant activity (86% at a concentration of 10 mg/mL) and positive prebiotic activity (2.27–2.67). DGP extracted and purified from Grateloupia gibbesii Harvey can be considered as a natural source contestant in the treatment of thrombosis and as an antioxidant and prebiotic supplement in the drug and food industries.
In the present study, the whole chloroplast (cp) genome of B. marginata was characterized for the first time and genomic features were comparatively analyzed with six relative species in Ulvales. The cp genome of B. marginata was 170, 562 bp in length, exhibiting similar general structure but different in GC content from Ulva and Pseudendoclonium. A total of 113 unique genes were annotated, including 84 protein-coding genes, 26 tRNA and 3 rRNA. A higher level of rearrangements and small syntenic blocks exists comparing the locally collinear blocks. Codon usage analysis identified 30 biased codons with A or U-ended. Sequence analysis detected a total of 23 forward repeats, 18 palindrome repeats, 8 reverse repeats and 38 SSRs with different types. The phylogenetic analyses based on the entire cp genome suggested that Blidingia is closer to Ulva than to Pseudendoclonium. The entire cp genome of Blidingia provides a valuable resource for further studies.
The diatoms evolved within the stramenopiles, an ecologically important and diverse assemblage of eukaryotes that includes both photosynthetic macrophytes and microalgae, as well as non-photosynthetic heterotrophs and parasites. The evolutionary history of the stramenopiles, which stretches back to the Palaeozoic, has been marked by the acquisition of chloroplasts in a recent common ancestor of their photosynthetic members, the ochrophytes; and progressive gains of genes in the nuclear genome by horizontal and endosymbiotic gene transfer. Here, we place diatoms in their actual evolutionary context within the stramenopiles; identify gene transfers that have shaped the coding content of the diatom nucleus; and profile sources of differences in chloroplast and mitochondrial genome content between different stramenopiles including diatoms. We underline the importance of considering diatoms as evolutionary mosaics, supported by genes of bacterial, red, green and other eukaryotic algal origins, as illustrated by multiple phylogenomic studies realised over the last two decades; and the relatively limited changes to organelle genome content in diatoms compared to other stramenopile lineages. We further identify a previously undocumented transfer of a novel open reading frame of the chloroplasts of green algae into the ochrophytes, underlining the importance of changes in organelle and nuclear gene content, in defining the current biology of diatoms.KeywordsHorizontal gene transferEndosymbiosisShopping bag modelCryptomonadsHaptophytesDinoflagellates
Subphylum Cyanidiophytina is composed of a single class (Cyanidiophyceae) and three genera have been traditionally recognized: Cyanidium and Galdieria (Cyanidiales) and Cyanidioschyzon (Cyanidioschyzogonales); a new genus (Cyanidiococcus) has been recently described in the order Cyanidioschyzogonales. All species are exclusive to inland habitats, occurring mostly in thermal waters, as thermoacidophiles, and also as mesophiles (aerophytic or endolithic). Subphylum Proteorhodophytina is represented in freshwaters by all four classes (Compsopogonophyceae, Porphyrideophyceae, Rhodellophyceae, and Stylonematophyceae). Class Compsopogonophyceae has three freshwater members in the single order Compsopogonales: genera Boldia (family Boldiaceae), Compsopogon and Pulvinaster (family Compsopogonaceae); all are monospecific. Class Stylonematophyceae is represented by five genera, four in the order Stylonematales, Chroodactylon (one species), Chroothece (four species), Kyliniella and Rhodospora (one species), and one in the order Rufusiales, the monospecific genus Rufusia. Class Porphyridiophyceae has freshwater members in the genera Flintiella (one species) and Porphyridium (three species). Class Rhodellophyceae has the monospecific genus Glaucosphaera.
Marine intertidal macroalgae live in a highly variable environment, currently threatened by human activities which lead to ongoing changes on marine ecosytems worldwide. In this regard, algal populations have to adapt to an evolving environment to avoid disappearance, by migrating or producing particular metabolites for example.Besides, each species has a different adaptive capacity, the species presenting a high phenotypic plasticity being more likely to adapt to future environmental conditions than others. In this context, the aim of this work was to study the acclimation abilities of five macroalgal species (either native or introduced) from Brittany (France), through a one-year monitoring combining both ecological and metabolomic data. The first part focused on red macroalgae and mycosporine-like amino acids. Results suggested that these highly diverse compounds, whose synthesis pathway is not completely elucided, could be multifunctional secondary metabolites. Thus, they could play a key role in the future adaptation of some red algal species such as the native Palmaria palmata, compared to the introduced Grateloupia turuturu.The second part then focused on three species of brown macroalgae (Sargassaceae) and showed that the native Halidrys siliquosa is more threatened than the other native species (i.e. Bifurcaria bifurcata) in the context of global change. Indeed, it is a cold-water affinity species that is all the more threatened as it have to cope both with global change and co-habitation with introduced species such as Sargassum muticum.
Endosymbiosis is a relationship between two organisms wherein one cell resides inside the other. This affiliation, when stable and beneficial for the ‘host’ cell, can result in massive genetic innovation with the foremost examples being the evolution of eukaryotic organelles, the mitochondria and plastids. Despite its critical evolutionary role, there is limited knowledge about how endosymbiosis is initially established and how host–endosymbiont biology is integrated. Here, we explore this issue, using as our model the rhizarian amoeba Paulinella, which represents an independent case of primary plastid origin that occurred c. 120 million yr ago. We propose the ‘chassis and engine’ model that provides a theoretical framework for understanding primary plastid endosymbiosis, potentially explaining why it is so rare.
Astaxanthin is arguably nature's most potent antioxidant, powerful to prevent free radical damage and oxidative stress. The microalga Haematococcus pluvialis seems to accumulate the highest levels of astaxanthin in nature and thus is currently the primary industrial source for natural astaxanthin production. The accumulation happens under photooxidative stress to quench radical damage from the photosynthesis, which is considered as one of the main reasons why chloroplast genomes are usually kept the small size and high guanine-cytosine (GC) content. We hypothesize that the outstanding astaxanthin production of the species may reflect its chloroplast genome features. In this study, the complete chloroplast genome of H. pluvialis FACHB-712 was sequenced and investigated. The genome is large, comprising 1.35 Mbp with 83 genes. However, the GC content is counterintuitively as high as 50.1%. The genome shows slight phylogenetic distance and genome structural differences in comparison with that of H. lacustris, whose species nomenclature is confusing and controversial. Moreover, a possible correlation between its powerful antioxidant capacity and the large chloroplast genome maintenance was further investigated. Strains of Chlorophyta and several strains with chloroplast genomes size of more than 500 kbp were used for comparative analysis. The evolutionary mechanism for the large chloroplast genome and and the contribution of non-coding region ratio and GC content to genome amplification is discussed.Large genomes may be associated with harsh habitats, and increased GC content may be used to increase stability.
In modern oceans, eukaryotic phytoplankton is dominated by lineages with red algal-derived plastids such as diatoms, dinoflagellates, and coccolithophores. Despite the ecological importance of these groups and many others representing a huge diversity of forms and lifestyles, we still lack a comprehensive understanding of their evolution and how they obtained their plastids. New hypotheses have emerged to explain the acquisition of red algal-derived plastids by serial endosymbiosis, but the chronology of these putative independent plastid acquisitions remains untested. Here, we establish a timeframe for the origin of red algal-derived plastids under scenarios of serial endosymbiosis, using Bayesian molecular clock analyses applied on a phylogenomic dataset with broad sampling of eukaryote diversity. We find that the hypotheses of serial endosymbiosis are chronologically possible, as the stem lineages of all red plastid-containing groups overlap in time. This period in the Meso- and Neoproterozoic Eras set the stage for the later expansion to dominance of red algal-derived primary production in the contemporary oceans, which profoundly altered the global geochemical and ecological conditions of the Earth.
The advent of high‐throughput‐sequencing (HTS) has allowed for the use of large numbers of coding regions to produce robust phylogenies. These phylogenies have been used to highlight relationships at ancient diversifications (subphyla, class), and highlight the evolution of plastid genome structure. The Erythropeltales are an order in the Compsopogonophyceae, a group with unusual plastid genomes but with low taxon sampling. We use HTS to produce near complete plastid genomes of all genera, and multiple species within some genera, to produce robust phylogenies to investigate character evolution, dating of divergence in the group, and plastid organization, including intron patterns. Our results produce a fully supported phylogeny of the genera in the Erythropeltales, and suggest that morphologies (upright versus crustose) have evolved multiple times. Our dated phylogeny also indicates that the order is very old (~ 800 Ma), with diversification occurring after the ice ages of the Cryogenian period (750‐635 Ma). Plastid gene order is congruent with phylogenetic relationships and suggests that genome architecture does not change often. Our data also highlight the abundance of introns in the plastid genomes of this order. We also produce a nearly complete plastid genome of Tsunamia transpacifica (Stylonematophyceae) to add to the taxon sampling of genomes of this class. The use of plastid genomes clearly produces robust phylogenetic relationships that can be used to infer evolutionary events, and increased taxon sampling, especially in less well‐known red algal groups, will provide additional insights into their evolution.
Evolution has led to a great diversity that ranges from elegant simplicity to ornate complexity. Many complex features are often assumed to be more functional or adaptive than their simpler alternatives. However, in 1999, Arlin Stolzfus published a paper in the Journal of Molecular Evolution that outlined a framework in which complexity can arise through a series of non-adaptive steps. He called this framework Constructive Neutral Evolution (CNE). Despite its two-decade-old roots, many evolutionary biologists still appear to be unaware of this explanastory framework for the origins of complexity. In this perspective piece, we explain the theory of CNE and how it changes the order of events in narratives that describe the evolution of complexity. We also provide an extensive list of cellular features that may have become more complex through CNE. We end by discussing strategies to determine whether complexity arose through neutral or adaptive processes.
The haptophyte Isochrysis galbana is an algal species of commercial interest due to its ability to accumulate high levels of fucoxanthin. In this study, the complete chloroplast (cp) genome of I. galbana was sequenced using a combination of Illumina and third-generation sequencing platforms. This circular cp genome was 105,872 bp in length, consisting of a large single-copy (LSC) region of 54,838 bp and a small single-copy (SSC) region of 41,308 bp separated by two direct rDNA repeats of 4862 bp and 4864 bp. The cp genome contained 141 unique genes, including 112 protein-coding genes with no introns, 26 transfer-RNA (tRNA) genes and three ribosomal-RNA (rRNA) genes. Like canonical ribosomal operon repeat structure, two 16S-trnI-trnA-23S-5S ribosomal RNA operons were identified. A total of 32 pairs of small repeats and 45 perfect microsatellites were detected. All haptophyte chloroplasts sequenced to date apart from E. huxleyi have either a complete pair of canonical repeats with direct orientation or noncanonical inverted repeats that lost part of tRNAs, or they have lost the inverted repeat arrangement altogether. Additionally, imperfect ribosomal operon repeats were observed in most haptophytes. The non-identical 4.9 kb ribosomal direct-repeats in I. galbana cp genome were distinguished by three 1–2 bp-sized inserts/deletions (InDels) and 32 single nucleotide polymorphisms (SNPs). Pairwise chloroplast genome comparisons showed a high degree of conservation in genome structure, gene order and gene content between I. galbana and T. lutea, with an overall SNP mutation rate of 4.3 × 10⁻³ per site. Only 458 SNPs, 18 small InDels and one large insertion were detected between these two cp genomes. The transition-to-transversion (Ts/Tv) ratio was 1.79 and the predominant mutations were A/T to G/C transitions. Phylogenetic analysis of currently available haptophyte chloroplasts also reflected that I. galbana was most closely related to T. lutea. The Ka/Ks ratios of shared genes in Isochrysidales chloroplast genomes were less than 1, suggesting that those genes are under purifying selection. The phylogenetic tree yielded by plastome single-copy orthologous genes gives new evidence on the relationships among CASH lineages. This first I. galbana chloroplast genome will provide insight into the chloroplast architecture, function and evolution of this species and other haptophytes.
Red algae comprise an anciently diverged, species-rich phylum with morphologies that span unicells to large seaweeds. Here, leveraging a rich red algal genome and transcriptome dataset, we used 298 single-copy orthologous nuclear genes from 15 red algal species to erect a robust multi-gene phylogeny of Rhodophyta. This tree places red seaweeds (Bangiophyceae and Florideophyceae) at the base of the mesophilic red algae with the remaining non-seaweed mesophilic lineages forming a well-supported sister group. The early divergence of seaweeds contrasts with the evolution of multicellular land plants and brown algae that are nested among multiple, unicellular or filamentous sister lineages. Using this novel perspective on red algal evolution, we studied the evolution of the pathways for isoprenoid biosynthesis. This analysis revealed losses of the mevalonate pathway on at least three separate occasions in lineages that contain Cyanidioschyzon, Porphyridium, and Chondrus. Our results establish a framework for in-depth studies of the origin and evolution of genes and metabolic pathways in Rhodophyta.
Background:
The red algae (Rhodophyta) diverged from the green algae and plants (Viridiplantae) over one billion years ago within the kingdom Archaeplastida. These photosynthetic lineages provide an ideal model to study plastid genome reduction in deep time. To this end, we assembled a large dataset of the plastid genomes that were available, including 48 from the red algae (17 complete and three partial genomes produced for this analysis) to elucidate the evolutionary history of these organelles.
Results:
We found extreme conservation of plastid genome architecture in the major lineages of the multicellular Florideophyceae red algae. Only three minor structural types were detected in this group, which are explained by recombination events of the duplicated rDNA operons. A similar high level of structural conservation (although with different gene content) was found in seed plants. Three major plastid genome architectures were identified in representatives of 46 orders of angiosperms and three orders of gymnosperms.
Conclusions:
Our results provide a comprehensive account of plastid gene loss and rearrangement events involving genome architecture within Archaeplastida and lead to one over-arching conclusion: from an ancestral pool of highly rearranged plastid genomes in red and green algae, the aquatic (Florideophyceae) and terrestrial (seed plants) multicellular lineages display high conservation in plastid genome architecture. This phenomenon correlates with, and could be explained by, the independent and widely divergent (separated by >400 million years) origins of complex sexual cycles and reproductive structures that led to the rapid diversification of these lineages.
The integration of foreign DNA into algal and plant plastid genomes is a rare event, with only a few known examples of horizontal gene transfer (HGT). Plasmids, which are well-studied drivers of HGT in prokaryotes, have been reported previously in red algae (Rhodophyta). However, the distribution of these mobile DNA elements and their sites of integration into the plastid (ptDNA), mitochondrial (mtDNA), and nuclear genomes of Rhodophyta remain unknown. Here we reconstructed the complex evolutionary history of plasmid-derived DNAs in red algae. Comparative analysis of 21 rhodophyte ptDNAs, including new genome data for 5 species, turned up 22 plasmid-derived open reading frames (ORFs) that showed syntenic and copy number variation among species, but were conserved within different individuals in three lineages. Several plasmid-derived homologs were found not only in ptDNA but also in mtDNA and in the nuclear genome of green plants, stramenopiles, and rhizarians. Phylogenetic and plasmid-derived ORF analyses showed that the majority of plasmid DNAs originated within red algae, whereas others were derived from cyanobacteria, other bacteria, and viruses. Our results elucidate the evolution of plasmid DNAs in red algae and suggest that they spread as parasitic genetic elements. This hypothesis is consistent with their sporadic distribution within Rhodophyta.
The Florideophyceae is the most abundant and taxonomically diverse class of red algae (Rhodophyta). However, many aspects of the systematics and divergence times of the group remain unresolved. Using a seven-gene concatenated dataset (nuclear EF2, LSU and SSU rRNAs, mitochondrial cox1, and plastid rbcL, psaA and psbA genes), we generated a robust phylogeny of red algae to provide an evolutionary timeline for florideophyte diversification. Our relaxed molecular clock analysis suggests that the Florideophyceae diverged approximately 943 (817–1,049) million years ago (Ma). The major divergences in this class involved the emergence of Hildenbrandiophycidae [ca. 781 (681–879) Ma], Nemaliophycidae [ca. 661 (597–736) Ma], Corallinophycidae [ca. 579 (543–617) Ma], and the split of Ahnfeltiophycidae and Rhodymeniophycidae [ca. 508 (442–580) Ma]. Within these clades, extant diversity reflects largely Phanerozoic diversification. Divergences within Florideophyceae were accompanied by evolutionary changes in the carposporophyte stage, leading to a successful strategy for maximizing spore production from each fertilization event. Our research provides robust estimates for the divergence times of major lineages within the Florideophyceae. This timeline was used to interpret the emergence of key morphological innovations that characterize these multicellular red algae.
Assembling the global eukaryotic tree of life has long been a major effort of Biology. In recent years, pushed by the new availability of genome-scale data for microbial eukaryotes, it has become possible to revisitmany evolutionary enigmas. However, some of the most ancient nodes, which are essential for inferring a stable tree, have remained highly controversial. Among other reasons, the lack of adequate genomic datasets for key taxa has prevented the robust reconstruction of early diversification events. In this context, the centrohelid heliozoans are particularly relevant for reconstructing the tree of eukaryotes because they represent one of the last substantial groups that was missing large and diverse genomic data. Here,we filled this gap by sequencing high-quality transcriptomes for four centrohelid lineages, each corresponding to a different family. Combining these new data with a broad eukaryotic sampling, we produced a gene-rich taxon-rich phylogenomic dataset that enabled us to refine the structure of the tree. Specifically, we show that (i) centrohelids relate to haptophytes, confirming Haptista; (ii) Haptista relates to SAR; (iii) Cryptista share strong affinity with Archaeplastida; and (iv) Haptista + SAR is sister to Cryptista + Archaeplastida. The implications of this topology are discussed in the broader context of plastid evolution. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
Group II introns are closely linked to eukaryote evolution because nuclear spliceosomal introns and the small RNAs associated with the spliceosome are thought to trace their ancient origins to these mobile elements. Therefore, elucidating how group II introns move, and how they lose mobility can potentially shed light on fundamental aspects of eukaryote biology. To this end, we studied five strains of the unicellular red alga Porphyridium purpureum that surprisingly contain 42 group II introns in their plastid genomes. We focused on a subset of these introns that encode mobility-conferring intron-encoded proteins (IEPs) and found them to be distributed among the strains in a lineage-specific manner. The reverse transcriptase and maturase domains were present in all lineages but the DNA endonuclease domain was deleted in vertically inherited introns, demonstrating a key step in the loss of mobility. P. purpureum plastid intron RNAs had a classic group IIB secondary structure despite variability in the DIII and DVI domains. We report for the first time the presence of twintrons (introns-within-introns, derived from the same mobile element) in Rhodophyta. The P. purpureum IEPs and their mobile introns provide a valuable model for the study of mobile retroelements in eukaryotes and offer promise for biotechnological applications.
Algae with secondary plastids of a red algal origin, such as ochrophytes (photosynthetic stramenopiles), are diverse and ecologically important, yet their evolutionary history remains controversial. We sequenced plastid genomes of two ochrophytes, Ochromonas sp. CCMP1393 (Chrysophyceae) and Trachydiscus minutus (Eustigmatophyceae). A shared split of the clpC gene as well as phylogenomic analyses of concatenated protein sequences demonstrated that chrysophytes and eustigmatophytes form a clade, the Limnista, exhibiting an unexpectedly elevated rate of plastid gene evolution. Our analyses also indicate that the root of the ochrophyte phylogeny falls between the recently redefined Khakista and Phaeista assemblages. Taking advantage of the expanded sampling of plastid genome sequences, we revisited the phylogenetic position of the plastid of Vitrella brassicaformis, a member of Alveolata with the least derived plastid genome known for the whole group. The results varied depending on the dataset and phylogenetic method employed, but suggested that the Vitrella plastids emerged from a deep ochrophyte lineage rather than being derived vertically from a hypothetical plastid-bearing common ancestor of alveolates and stramenopiles. Thus, we hypothesize that the plastid in Vitrella, and potentially in other alveolates, may have been acquired by an endosymbiosis of an early ochrophyte.
We present a consensus classification of life to embrace the more than 1.6 million species already provided by more than 3,000 taxonomists' expert opinions in a unified and coherent, hierarchically ranked system known as the Catalogue of Life (CoL). The intent of this collab-orative effort is to provide a hierarchical classification serving not only the needs of the CoL's database providers but also the diverse public-domain user community, most of whom are familiar with the Linnaean conceptual system of ordering taxon relationships. This classification is neither phylogenetic nor evolutionary but instead represents a consensus view that accommodates taxonomic choices and practical compromises among diverse expert opinions, public usages, and conflicting evidence about the boundaries between taxa and the ranks of major taxa, including kingdoms. Certain key issues, some not fully resolved , are addressed in particular. Beyond its immediate use as a management tool for the CoL and ITIS (Integrated Taxonomic Information System), it is immediately valuable as a reference for taxonomic and biodiversity research, as a tool for societal communication, and as a classificatory " backbone " for biodiversity databases, museum collections, libraries, and textbooks. Such a modern comprehensive hierarchy has not previously existed at this level of specificity.
Species of Bryopsidales form ecologically important components of seaweed communities worldwide. These siphonous macroalgae are composed of a single giant tubular cell containing millions of nuclei and chloroplasts, and harbor diverse bacterial communities. Little is known about the diversity of chloroplast genomes (cpDNAs) in this group, and about the possible consequences of intracellular bacteria on genome composition of the host. We present the complete cpDNAs of Bryopsis plumosa and Tydemania expeditionis, as well as a re-annotated cpDNA of B. hypnoides, which was shown to contain a higher number of genes than originally published. Chloroplast genomic data were also used to evaluate phylogenetic hypotheses in the Chlorophyta, such as monophyly of the Ulvophyceae (the class in which the order Bryopsidales is currently classified).
Both DNAs are circular and lack a large inverted repeat. The cpDNA of B. plumosa is 106,859 bp long and contains 115 unique genes. A 13 kb region was identified with several freestanding open reading frames (ORFs) of putative bacterial origin, including a large ORF (>8 kb) closely related to bacterial rhs-family genes. The cpDNA of T. expeditionis is 105,200 bp long and contains 125 unique genes. As in B. plumosa, several regions were identified with ORFs of possible bacterial origin, including genes involved in mobile functions (transposases, integrases, phage/plasmid DNA primases), and ORFs showing close similarity with bacterial DNA methyltransferases. The cpDNA of B. hypnoides differs from that of B. plumosa mainly in the presence of long intergenic spacers, and a large tRNA region. Chloroplast phylogenomic analyses were largely inconclusive with respect to monophyly of the Ulvophyceae, and the relationship of the Bryopsidales within the Chlorophyta.
The cpDNAs of B. plumosa and T. expeditionis are amongst the smallest and most gene dense chloroplast genomes in the core Chlorophyta. The presence of bacterial genes, including genes typically found in mobile elements, suggest that these have been acquired through horizontal gene transfer, which may have been facilitated by the occurrence of obligate intracellular bacteria in these siphonous algae.
Mitochondrial and plastid genomes show a wide array of architectures, varying immensely in size, structure, and content. Some organelle DNAs have even developed elaborate eccentricities, such as scrambled coding regions, nonstandard genetic codes, and convoluted modes of posttranscriptional modification and editing. Here, we compare and contrast the breadth of genomic complexity between mitochondrial and plastid chromosomes. Both organelle genomes have independently evolved many of the same features and taken on similar genomic embellishments, often within the same species or lineage. This trend is most likely because the nuclear-encoded proteins mediating these processes eventually leak from one organelle into the other, leading to a high likelihood of processes appearing in both compartments in parallel. However, the complexity and intensity of genomic embellishments are consistently more pronounced for mitochondria than for plastids, even when they are found in both compartments. We explore the evolutionary forces responsible for these patterns and argue that organelle DNA repair processes, mutation rates, and population genetic landscapes are all important factors leading to the observed convergence and divergence in organelle genome architecture.
Large phylogenomics data sets require fast tree inference methods, especially for maximum-likelihood (ML) phylogenies. Fast
programs exist, but due to inherent heuristics to find optimal trees, it is not clear whether the best tree is found. Thus,
there is need for additional approaches that employ different search strategies to find ML trees and that are at the same
time as fast as currently available ML programs. We show that a combination of hill-climbing approaches and a stochastic perturbation
method can be time-efficiently implemented. If we allow the same CPU time as RAxML and PhyML, then our software IQ-TREE found
higher likelihoods between 62.2% and 87.1% of the studied alignments, thus efficiently exploring the tree-space. If we use
the IQ-TREE stopping rule, RAxML and PhyML are faster in 75.7% and 47.1% of the DNA alignments and 42.2% and 100% of the protein
alignments, respectively. However, the range of obtaining higher likelihoods with IQ-TREE improves to 73.3–97.1%. IQ-TREE
is freely available at http://www.cibiv.at/software/iqtree.
Although many NGS read pre-processing tools already existed, we could not find any tool or combination of tools which met our requirements in terms of flexibility, correct handling of paired-end data, and high performance. We have developed Trimmomatic as a more flexible and efficient pre-processing tool, which could correctly handle paired-end data.
The value of NGS read pre-processing is demonstrated for both reference-based and reference-free tasks. Trimmomatic is shown to produce output which is at least competitive with, and in many cases superior to, that produced by other tools, in all scenarios tested.
Trimmomatic is licensed under GPL V3. It is cross-platform (Java 1.5+ required) and available from http://www.usadellab.org/cms/index.php?page=trimmomatic CONTACT: usadel@bio1.rwth-aachen.de SUPPLEMENTARY INFORMATION: Manual and source code are available from http://www.usadellab.org/cms/index.php?page=trimmomatic.
Phylogenies are increasingly used in all fields of medical and biological research. Moreover, because of the next generation sequencing revolution, datasets used for conducting phylogenetic analyses grow at an unprecedented pace. RAxML (Randomized Axelerated Maximum Likelihood) is a popular program for phylogenetic analyses of large datasets under maximum likelihood. Since the last RAxML paper in 2006, it has been continuously maintained and extended to accommodate the increasingly growing input datasets and to serve the needs of the user community.
I present some of the most notable new features and extensions of RAxML, such as, a substantial extension of substitution models and supported data types, the introduction of SSE3, AVX, and AVX2 vector intrinsics, techniques for reducing the memory requirements of the code and a plethora of operations for conducting post-analyses on sets of trees. In addition, an up-to-date, 50 page user manual covering all new RAxML options is available.
The code is available under GNU GPL at https://github.com/stamatak/standard-RAxML.
Alexandros.Stamatakis@h-its.org.
Plastids sequestered by sacoglossan sea slugs have long been a puzzle. Some sacoglossans feed on siphonaceous algae and can retain the plastids in the cytosol of their digestive gland cells. There, the stolen plastids (kleptoplasts) can remain photosynthetically active in some cases for months. Kleptoplast longevity itself challenges current paradigms concerning photosystem turnover, because kleptoplast photosystems remain active in the absence of nuclear algal genes. In higher plants, nuclear genes are essential, in particular for the constant repair of the D1 protein of photosystem II. Lateral gene transfer was long suspected to underpin slug kleptoplast longevity, but recent transcriptomic and genomic analyses show that no algal nuclear genes are expressed from the slug nucleus. Kleptoplast genomes themselves, however, appear expressed in the sequestered state. Here we present sequence data for the chloroplast genome of Acetabularia acetabulum, the food source of the sacoglossan Elysia timida, which can maintain Acetabularia kleptoplasts in an active state for months. The data reveal what might be the key to sacoglossan kleptoplast longevity: plastids that remain photosynthetically active within slugs for periods of months share the property of encoding ftsH, a D1 quality control protease that is essential for photosystem II repair. In land plants, ftsH is always nuclear encoded, it was transferred to the nucleus from the plastid genome when Charophyta and Embryophyta split. A replenishable supply of ftsH could, in principle, rescue kleptoplasts from D1 photodamage, thereby influencing plastid longevity in sacoglossan slugs.
Red algal systematics has a solid morphological foundation, based on analyses of female repro- ductive structures and post-fertilization development by Kylin and other workers. Recognition of the value of pit-plug ultrastructure was a catalyst leading to refinement of the Kylinian ordinal classification. Molecular approaches to systematics have further advanced our understanding of the red algae at every level and led to the proposal of several new orders. Species diversity in particular has traditionally been underestimated due to the presence of cryptic and pseudo-cryptic species.
Pyropia haitanensis and P. yezoensis are two economically important marine crops that are also considered to be research models to study the physiological ecology of intertidal seaweed communities, evolutionary biology of plastids, and the origins of sexual reproduction. This plastid genome information will facilitate study of breeding, population genetics and phylogenetics.
We have fully sequenced using next-generation sequencing the circular plastid genomes of P. hatanensis (195,597 bp) and P. yezoensis (191,975 bp), the largest of all the plastid genomes of the red lineage sequenced to date. Organization and gene contents of the two plastids were similar, with 211-213 protein-coding genes (including 29-31 unknown-function ORFs), 37 tRNA genes, and 6 ribosomal RNA genes, suggesting a largest coding capacity in the red lineage. In each genome, 14 protein genes overlapped and no interrupted genes were found, indicating a high degree of genomic condensation. Pyropia maintain an ancient gene content and conserved gene clusters in their plastid genomes, containing nearly complete repertoires of the plastid genes known in photosynthetic eukaryotes. Similarity analysis based on the whole plastid genome sequences showed the distance between P. haitanensis and P. yezoensis (0.146) was much smaller than that of Porphyra purpurea and P. haitanensis (0.250), and P. yezoensis (0.251); this supports re-grouping the two species in a resurrected genus Pyropia while maintaining P. purpurea in genus Porphyra. Phylogenetic analysis supports a sister relationship between Bangiophyceae and Florideophyceae, though precise phylogenetic relationships between multicellular red alage and chromists were not fully resolved.
These results indicate that Pyropia have compact plastid genomes. Large coding capacity and long intergenic regions contribute to the size of the largest plastid genomes reported for the red lineage. Possessing the largest coding capacity and ancient gene content yet found reveal that Pyropia are more primitive multicellular red algae.
Mitochondria and plastids (chloroplasts) are cell organelles of endosymbiotic origin that possess their own genetic information.
Most organellar DNAs map as circular double-stranded genomes. Across the eukaryotic kingdom, organellar genomes display great
size variation, ranging from ∼15 to 20 kb (the size of the mitochondrial genome in most animals) to >10 Mb (the size of the
mitochondrial genome in some lineages of flowering plants). We have developed OrganellarGenomeDraw (OGDRAW), a suite of software
tools that enable users to create high-quality visual representations of both circular and linear annotated genome sequences
provided as GenBank files or accession numbers. Although all types of DNA sequences are accepted as input, the software has
been specifically optimized to properly depict features of organellar genomes. A recent extension facilitates the plotting
of quantitative gene expression data, such as transcript or protein abundance data, directly onto the genome map. OGDRAW has
already become widely used and is available as a free web tool (http://ogdraw.mpimp-golm.mpg.de/). The core processing components can be downloaded as a Perl module, thus also allowing for convenient integration into custom
processing pipelines.
Modeling across site variation of the substitution process is increasingly recognized as important for obtaining more accurate phylogenetic reconstructions. Both finite and infinite mixture models have been proposed, and have been shown to significantly improve on classical single-matrix models. Compared to their finite counterparts, infinite mixtures have a greater expressivity. However, they are computationally more challenging. This has resulted in practical compromises in the design of infinite mixture models. In particular, a fast but simplified version of a Dirichlet process model over equilibirum frequency profiles implemented in PhyloBayes (Lartillot et al, 2007) has often been used in recent phylogenomics studies, while more refined model structures, more realistic and empirically more fit, have been practically out of reach.We introduce an Message Passing Interface (MPI) version of PhyloBayes, implementing the Dirichlet process mixture models as well as more classical empirical matrices and finite mixtures. The parallelization is made efficient thanks to the combination of two algorithmic strategies: a partial Gibbs sampling update of the tree topology, and the use of a truncated stick-breaking representation for the Dirichlet process prior. The implementation shows close to linear gains in computational speed for up to 64 cores, thus allowing faster phylogenetic reconstruction under complex mixture models.PhyloBayes MPI is freely available from our website www.phylobayes.org.
Red algae have the most gene-rich plastid genomes known, but despite their evolutionary importance these genomes remain poorly sampled. Here we characterize three complete and one partial plastid genome from a diverse range of florideophytes. By unifying annotations across all available red algal plastid genomes we show they all share a highly compact and slowly-evolving architecture and uniquely rich gene complements. Both chromosome structure and gene content have changed very little during red algal diversification, and suggest that plastid-to nucleus gene transfers have been rare. Despite their ancient character, however, the red algal plastids also contain several unprecedented features, including a group II intron in a tRNA-Met gene that encodes the first example of red algal plastid intron maturase - a feature uniquely shared among florideophytes. We also identify a rare case of a horizontally-acquired proteobacterial operon, and propose this operon may have been recruited for plastid function and potentially replaced a nucleus-encoded plastid-targeted paralogue. Plastid genome phylogenies yield a fully resolved tree and suggest that plastid DNA is a useful tool for resolving red algal relationships. Lastly, we estimate the evolutionary rates among more than 200 plastid genes, and assess their usefulness for species and subspecies taxonomy by comparison to well-established barcoding markers such as cox1 and rbcL. Overall, these data demonstrates that red algal plastid genomes are easily obtainable using high-throughput sequencing of total genomic DNA, interesting from evolutionary perspectives, and promising in resolving red algal relationships at evolutionarily-deep and species/subspecies levels.
Nonparametric bootstrap has been a widely used tool in phylogenetic analysis to assess the clade support of phylogenetic trees.
However, with the rapidly growing amount of data, this task remains a computational bottleneck. Recently, approximation methods
such as the RAxML rapid bootstrap (RBS) and the Shimodaira–Hasegawa-like approximate likelihood ratio test have been introduced
to speed up the bootstrap. Here, we suggest an ultrafast bootstrap approximation approach (UFBoot) to compute the support
of phylogenetic groups in maximum likelihood (ML) based trees. To achieve this, we combine the resampling estimated log-likelihood
method with a simple but effective collection scheme of candidate trees. We also propose a stopping rule that assesses the
convergence of branch support values to automatically determine when to stop collecting candidate trees. UFBoot achieves a
median speed up of 3.1 (range: 0.66–33.3) to 10.2 (range: 1.32–41.4) compared with RAxML RBS for real DNA and amino acid alignments,
respectively. Moreover, our extensive simulations show that UFBoot is robust against moderate model violations and the support
values obtained appear to be relatively unbiased compared with the conservative standard bootstrap. This provides a more direct
interpretation of the bootstrap support. We offer an efficient and easy-to-use software (available at http://www.cibiv.at/software/iqtree) to perform the UFBoot analysis with ML tree inference.
We present SequenceMatrix, software that is designed to facilitate the assembly and analysis of multi-gene datasets. Genes are concatenated by dragging and dropping FASTA, NEXUS, or TNT files with aligned sequences into the program window. A multi-gene dataset is concatenated and displayed in a spreadsheet; each sequence is represented by a cell that provides information on sequence length, number of indels, the number of ambiguous bases (“Ns”), and the availability of codon information. Alternatively, GenBank numbers for the sequences can be displayed and exported. Matrices with hundreds of genes and taxa can be concatenated within minutes and exported in TNT, NEXUS, or PHYLIP formats, preserving both character set and codon information for TNT and NEXUS files. SequenceMatrix also creates taxon sets listing taxa with a minimum number of characters or gene fragments, which helps assess preliminary datasets. Entire taxa, whole gene fragments, or individual sequences for a particular gene and species can be excluded from export. Data matrices can be re-split into their component genes and the gene fragments can be exported as individual gene files. SequenceMatrix also includes two tools that help to identify sequences that may have been compromised through laboratory contamination or data management error. One tool lists identical or near-identical sequences within genes, while the other compares the pairwise distance pattern of one gene against the pattern for all remaining genes combined. SequenceMatrix is Java-based and compatible with the Microsoft Windows, Apple MacOS X and Linux operating systems. The software is freely available from http://code.google.com/p/sequencematrix/.
© The Willi Hennig Society 2010.
Previous phylogenetic studies of the Rhodophyta have provided a framework for understanding red algal phylogeny, but there still exists the need for a comprehensive analysis using a broad sampling of taxa and sufficient phylogenetic information to clearly define the major lineages. In this study, we determined 48 sequences of the PSI P700 chl a apoprotein A1 (psaA) and rbcL coding regions and established a robust red algal phylogeny to identify the major clades. The tree included most of the lineages of the Bangiophyceae (25 genera, 48 taxa). Seven well-supported lineages were identified with this analysis with the Cyanidiales having the earliest divergence and being distinct from the remaining taxa; i.e. the Porphyridiales 1–3, Bangiales, Florideophyceae, and Compsopogonales. We also analyzed data sets with fewer taxa but using seven proteins or the DNA sequence from nine genes to resolve inter-clade relationships. Based on all of these analyses, we propose that the Rhodophyta contains two new subphyla, the Cyanidiophytina with a single class, the Cyanidiophyceae, and the Rhodophytina with six classes, the Bangiophyceae, Compsopogonophyceae, Florideophyceae, Porphyridiophyceae classis nov. (which contains Porphyridium, Flintiella, and Erythrolobus), Rhodellophyceae, and Stylonematophyceae classis nov. (which contains Stylonema, Bangiopsis, Chroodactylon, Chroothece, Purpureofilum, Rhodosorus, Rhodospora, and Rufusia). We also describe a new order, Rhodellales, and a new family, Rhodellaceae (with Rhodella, Dixoniella, and Glaucosphaera).
The red algae (Rhodophyta) form a distinct photosynthetic eukaryotic lineage that consists of around 6,000 species including
unicellular to large multicellular taxa (http://www.algaebase.org/). The red algae are unique among eukaryotes in lacking
both flagella and centrioles during their entire life cycle (Gabrielson et al., 1990; Graham and Wilcox, 2000). Pit connections,
pit plugs, and a triphasic life cycle that are mostly found in the Florideophyceae are also distinguishing characters of the
red algae. The photosynthetic organelle (plastid) of red algae is bounded by two membranes and contains chlorophyll-a, phycocyanin, and phycoerythrin as photosynthetic pigments. These pigment complexes, organized in phycobilisomes, are located
on the surface of unstacked thylakoid membranes to capture light energy. As a storage product, the red algae produce granulated
floridean starch in the cytoplasm that is different from green algal starch. In addition to these unique features, the monophyly
of red algae is strongly supported by nuclear, plastid, and mitochondrial gene trees (Freshwater et al., 1994; Ragan et al.,
1994; Van de Peer and De Wachter, 1997; Burger et al., 1999; Yoon et al., 2002b, 2004).
Summary: The two main functions of bioinformatics are the organization and analysis of biological data using computational resources. Geneious Basic has been designed to be an easy-to-use and flexible desktop software application framework for the organization and analysis of biological data, with a focus on molecular sequences and related data types. It integrates numerous industry-standard discovery analysis tools, with interactive visualizations to generate publication-ready images. One key contribution to researchers in the life sciences is the Geneious public application programming interface (API) that affords the ability to leverage the existing framework of the Geneious Basic software platform for virtually unlimited extension and customization. The result is an increase in the speed and quality of development of computation tools for the life sciences, due to the functionality and graphical user interface available to the developer through the public API. Geneious Basic represents an ideal platform for the bioinformatics community to leverage existing components and to integrate their own specific requirements for the discovery, analysis and visualization of biological data.Availability and implementation: Binaries and public API freely available for download at http://www.geneious.com/basic, implemented in Java and supported on Linux, Apple OSX and MS Windows. The software is also available from the Bio-Linux package repository at http://nebc.nerc.ac.uk/news/geneiousonbl.Contact:
peter@biomatters.com
The lion's share of bacteria in various environments cannot be cloned in the laboratory and thus cannot be sequenced using existing technologies. A major goal of single-cell genomics is to complement gene-centric metagenomic data with whole-genome assemblies of uncultivated organisms. Assembly of single-cell data is challenging because of highly non-uniform read coverage as well as elevated levels of sequencing errors and chimeric reads. We describe SPAdes, a new assembler for both single-cell and standard (multicell) assembly, and demonstrate that it improves on the recently released E+V-SC assembler (specialized for single-cell data) and on popular assemblers Velvet and SoapDeNovo (for multicell data). SPAdes generates single-cell assemblies, providing information about genomes of uncultivatable bacteria that vastly exceeds what may be obtained via traditional metagenomics studies. SPAdes is available online ( http://bioinf.spbau.ru/spades ). It is distributed as open source software.
We sequenced the nuclear small subunit ribosomal DNA coding region from 20 members of the Bangiophycidae and from two members of the Florideophycidae to gain insights into red algal evolution. A combined alignment of nuclear and plastid small subunit rDNA and a data set of Rubisco protein sequences were also studied to complement the understanding of bangiophyte phylogeny and to address red algal secondary symbiosis. Our results are consistent with a monophyletic origin of the Florideophycidae, which form a sister-group to the Bangiales. Bangiales monophyly is strongly supported, although Porphyra is polyphyletic within Bangia. Bangiophycidae orders such as the Porphyridiales are distributed over three independent red algal lineages. The Compsopogonales sensu stricto, consisting of two freshwater families, Compsopogonaceae and Boldiaceae, forms a well-supported monophyletic grouping. The single taxon within the Rhodochaetales, Rhodochaete parvula, is positioned within a cluster containing members of the Erythropeltidales. Analyses of Rubisco sequences show that the plastids of the heterokonts are most closely related to members of the Cyanidiales and are not directly related to cryptophyte and haptophyte plastid genomes. Our results support the independent origins of these secondary algal plastids from different members of the Bangiophycidae.
The quality of multiple sequence alignments plays an important role in the accuracy of phylogenetic inference. It has been shown that removing ambiguously aligned regions, but also other sources of bias such as highly variable (saturated) characters, can improve the overall performance of many phylogenetic reconstruction methods. A current scientific trend is to build phylogenetic trees from a large number of sequence datasets (semi-)automatically extracted from numerous complete genomes. Because these approaches do not allow a precise manual curation of each dataset, there exists a real need for efficient bioinformatic tools dedicated to this alignment character trimming step.
Here is presented a new software, named BMGE (Block Mapping and Gathering with Entropy), that is designed to select regions in a multiple sequence alignment that are suited for phylogenetic inference. For each character, BMGE computes a score closely related to an entropy value. Calculation of these entropy-like scores is weighted with BLOSUM or PAM similarity matrices in order to distinguish among biologically expected and unexpected variability for each aligned character. Sets of contiguous characters with a score above a given threshold are considered as not suited for phylogenetic inference and then removed. Simulation analyses show that the character trimming performed by BMGE produces datasets leading to accurate trees, especially with alignments including distantly-related sequences. BMGE also implements trimming and recoding methods aimed at minimizing phylogeny reconstruction artefacts due to compositional heterogeneity.
BMGE is able to perform biologically relevant trimming on a multiple alignment of DNA, codon or amino acid sequences. Java source code and executable are freely available at ftp://ftp.pasteur.fr/pub/GenSoft/projects/BMGE/.
The Chlorophyceae, an advanced class of chlorophyte green algae, comprises five lineages that form two major clades (Chlamydomonadales + Sphaeropleales and Oedogoniales + Chaetopeltidales + Chaetophorales). The four complete chloroplast DNA (cpDNA) sequences currently available for chlorophyceans uncovered an extraordinarily fluid genome architecture as well as many structural features distinguishing this group from other green algae. We report here the 521,168-bp cpDNA sequence from a member of the Chaetopeltidales (Floydiella terrestris), the sole chlorophycean lineage not previously sampled for chloroplast genome analysis. This genome, which contains 97 conserved genes and 26 introns (19 group I and 7 group II introns), is the largest chloroplast genome ever sequenced. Intergenic regions account for 77.8% of the genome size and are populated by short repeats. Numerous genomic features are shared with the cpDNA of the chaetophoralean Stigeoclonium helveticum, notably the absence of a large inverted repeat and the presence of unique gene clusters and trans-spliced group II introns. Although only one of the Floydiella group I introns encodes a homing endonuclease gene, our finding of five free-standing reading frames having similarity with such genes suggests that chloroplast group I introns endowed with mobility were once more abundant in the Floydiella lineage. Parsimony analysis of structural genomic features and phylogenetic analysis of chloroplast sequence data unambiguously resolved the Oedogoniales as sister to the Chaetopeltidales and Chaetophorales. An evolutionary scenario of the molecular events that shaped the chloroplast genome in the Chlorophyceae is presented.
Multiple genome alignment remains a challenging problem. Effects of recombination including rearrangement, segmental duplication, gain, and loss can create a mosaic pattern of homology even among closely related organisms.
We describe a new method to align two or more genomes that have undergone rearrangements due to recombination and substantial amounts of segmental gain and loss (flux). We demonstrate that the new method can accurately align regions conserved in some, but not all, of the genomes, an important case not handled by our previous work. The method uses a novel alignment objective score called a sum-of-pairs breakpoint score, which facilitates accurate detection of rearrangement breakpoints when genomes have unequal gene content. We also apply a probabilistic alignment filtering method to remove erroneous alignments of unrelated sequences, which are commonly observed in other genome alignment methods. We describe new metrics for quantifying genome alignment accuracy which measure the quality of rearrangement breakpoint predictions and indel predictions. The new genome alignment algorithm demonstrates high accuracy in situations where genomes have undergone biologically feasible amounts of genome rearrangement, segmental gain and loss. We apply the new algorithm to a set of 23 genomes from the genera Escherichia, Shigella, and Salmonella. Analysis of whole-genome multiple alignments allows us to extend the previously defined concepts of core- and pan-genomes to include not only annotated genes, but also non-coding regions with potential regulatory roles. The 23 enterobacteria have an estimated core-genome of 2.46Mbp conserved among all taxa and a pan-genome of 15.2Mbp. We document substantial population-level variability among these organisms driven by segmental gain and loss. Interestingly, much variability lies in intergenic regions, suggesting that the Enterobacteriacae may exhibit regulatory divergence.
The multiple genome alignments generated by our software provide a platform for comparative genomic and population genomic studies. Free, open-source software implementing the described genome alignment approach is available from http://gel.ahabs.wisc.edu/mauve.
The noncoding-DNA content of organelle and nuclear genomes can vary immensely. Both adaptive and nonadaptive explanations for this variation have been proposed. This study addresses a nonadaptive explanation called the mutational-hazard hypothesis and applies it to the mitochondrial, plastid, and nuclear genomes of the multicellular green alga Volvox carteri. Given the expanded architecture of the V. carteri organelle and nuclear genomes (60-85% noncoding DNA), the mutational-hazard hypothesis would predict them to have less silent-site nucleotide diversity (π(silent)) than their more compact counterparts from other eukaryotes-ultimately reflecting differences in 2N(g)μ (twice the effective number of genes per locus in the population times the mutation rate). The data presented here support this prediction: Analyses of mitochondrial, plastid, and nuclear DNAs from seven V. carteri forma nagariensis geographical isolates reveal low values of π(silent) (0.00038, 0.00065, and 0.00528, respectively), much lower values than those previously observed for the more compact organelle and nuclear DNAs of Chlamydomonas reinhardtii (a close relative of V. carteri). We conclude that the large noncoding-DNA content of the V. carteri genomes is best explained by the mutational-hazard hypothesis and speculate that the shift from unicellular to multicellular life in the ancestor that gave rise to V. carteri contributed to a low V. carteri population size and thus a reduced 2N(g)μ. Complete mitochondrial and plastid genome maps for V. carteri are also presented and compared with those of C. reinhardtii.
The assembly of the tree of life has seen significant progress in recent years but algae and protists have been largely overlooked in this effort. Many groups of algae and protists have ancient roots and it is unclear how much data will be required to resolve their phylogenetic relationships for incorporation in the tree of life. The red algae, a group of primary photosynthetic eukaryotes of more than a billion years old, provide the earliest fossil evidence for eukaryotic multicellularity and sexual reproduction. Despite this evolutionary significance, their phylogenetic relationships are understudied. This study aims to infer a comprehensive red algal tree of life at the family level from a supermatrix containing data mined from GenBank. We aim to locate remaining regions of low support in the topology, evaluate their causes and estimate the amount of data required to resolve them.
Phylogenetic analysis of a supermatrix of 14 loci and 98 red algal families yielded the most complete red algal tree of life to date. Visualization of statistical support showed the presence of five poorly supported regions. Causes for low support were identified with statistics about the age of the region, data availability and node density, showing that poor support has different origins in different parts of the tree. Parametric simulation experiments yielded optimistic estimates of how much data will be needed to resolve the poorly supported regions (ca. 103 to ca. 104 nucleotides for the different regions). Nonparametric simulations gave a markedly more pessimistic image, some regions requiring more than 2.8 105 nucleotides or not achieving the desired level of support at all. The discrepancies between parametric and nonparametric simulations are discussed in light of our dataset and known attributes of both approaches.
Our study takes the red algae one step closer to meaningful inclusion in the tree of life. In addition to the recovery of stable relationships, the recognition of five regions in need of further study is a significant outcome of this work. Based on our analyses of current availability and future requirements of data, we make clear recommendations for forthcoming research.
We describe a program, tRNAscan-SE, which identifies 99-100% of transfer RNA genes in DNA sequence while giving less than one false positive per 15 gigabases. Two previously described tRNA detection programs are used as fast, first-pass prefilters to identify candidate tRNAs, which are then analyzed by a highly selective tRNA covariance model. This work represents a practical application of RNA covariance models, which are general, probabilistic secondary structure profiles based on stochastic context-free grammars. tRNAscan-SE searches at approximately 30 000 bp/s. Additional extensions to tRNAscan-SE detect unusual tRNA homologues such as selenocysteine tRNAs, tRNA-derived repetitive elements and tRNA pseudogenes.
Algae are characterized by the presence of plastids (chloroplasts), which are organelles of cyanobacterial origin. Plastids have their own genome, machineries for replication, transcription and translation, and are the site of photosynthesis (except in secondarily non-photosynthetic species) and a variety of other biological functions. Algae are subdivided into those whose plastids can be traced back to a common cyanobacterial endosymbiont (algae with primary plastids), and others in which plastids are second-hand acquisitions that were introduced by eukaryote-eukaryote endosymbioses. Only a fraction of plastid components is encoded in plastid DNA; the majority of genes coding for plastid proteins are in the nucleus, many of which originated through transfers (in some cases still ongoing) from the organelle to the nuclear genome. Despite the broad phylogenetic affiliation of algae, most plastid genomes are fairly homogenous, coding for about 100–250 genes, except in non-photosynthetic algae that rapidly lose genes involved in photosynthesis. The most gene-rich and cyanobacteria-like plastid genomes are in red algae, followed by glaucophyte and green algae. Genomes in secondary or higher-order plastids usually have a reduced gene count, compared to their primary photosynthetic donors. In this chapter, we provide an overview on the evolutionary history, organization and coding properties of algal plastid genomes, for which complete (or almost complete) sequences are publicly available.
Over the last few years multiple studies have been published outlining chloroplast genomes that represent many of the photosynthetic euglenid genera. However, these genomes were scattered throughout the euglenophyceaean phylogenetic tree, and focused on comparisons with E. gracilis. Here, we present a study exclusively on taxa within the Euglenaceae. Six new chloroplast genomes were characterized, those of Cryptoglena skujai, Euglena gracilis var. bacillaris, Euglena viridis, Euglenaria anabaena, Monomorphina parapyrum, and Trachelomonas volvocina, and added to six previously published chloroplast genomes to determine if trends existed within the family. With this study: at least one genome has now been characterized for each genus, the genomes of different strains from two taxa were characterized to explore intra-specific variability, and a second taxon has been characterized for the genus Monomorphina to examine intra-generic variability. Overall results showed a large amount of variability among the genomes, though a few trends could be identified both within Euglenaceae and within Euglenophyta. In addition, the intra-specific analysis indicated that the similarity of a genome sequence between strains was taxon dependent, and the intra-generic analysis indicated that the majority of the evolutionary changes within the Euglenaceae occurred inter-generically. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Symbiogenesis is the extremely rare, but permanent merger of two organisms from phylogenetically distant lineages into one radically more complex organism. Three examples are exceptionally important: intracellular enslavement by an early eukaryote of an alpha-proteobacterium by host protein insertion to make mitochondria; later conversion of a cyanobacterium into the first chloroplast, thereby forming kingdom Plantae; and secondary enslavement of a red alga to yield more complex membrane topology in the phagophototrophic kingdom Chromista. Two other cases involved independent acquisition of green-algal chloroplasts by ancestrally phagotrophic lineages, yielding chlorarachnean algae (phylum Cercozoa, within the chromist infrakingdom Rhizaria) and euglenophyte algae (phylum Euglenozoa, within the protozoan subkingdom Eozoa). Less radically, chloroplast replacement occurred within dinoflagellate Chromista by two symbiogeneses: Green-algal or haptophyte chloroplasts replaced ancestral peridinin-containing chloroplasts. These seven lineage mergers were all mediated by the evolution of novel modes of transmembrane protein import into the enslaved cell, allowing massive gene transfer from symbionts to host genomes.
We present the 174,935 nt long plastid genome of the red alga Laurencia sp. JFC0032. It is the third plastid genome characterized for the largest order of red algae (Ceramiales). The circular-mapping plastid genome is small compared to most florideophyte red algae, and our comparisons show a trend towards smaller plastid genome sizes in the family Rhodomelaceae, independent from a similar trend in Cyanidiophyceae. The Laurencia genome is densely packed with 200 annotated protein-coding genes (188 widely conserved, 3 ORFs shared with other red algae and 9 hypothetical coding regions). It has 29 tRNAs, a single-copy ribosomal RNA cistron, a tmRNA and the RNase P RNA.
The authors report on the presence of a new alga (which appears to belong to the Rhodophyta) in the thermal acidic environments near the solfatane fumaroles of Campi Flegrei (Naples, Italy).On the ground of the microscopical observations, the authors emphasize that the characteristics of this alga are so peculiar as to consent the institution on it of a new genus Cyanidioschyzon and a new species; the authors therefore propose the name Cyanidioschyzon merolae. Gli autori hanno isolato, dalle fumarole dei Campi Flegrei (Napoli, Italia), un'alga unicellulare eucariota, acidofila e termofila, attribuibile alle Rhodophyta. Quest'alga ha forma di clava, è lunga 3–4 μ, ed è larga ca. 1,5 μ nella porzione slargata. Si divide longitudinalmente in due e non mostra fenomeni di gamia o di autosporia. L'alga, studiata al M.E., mostra all'estremità slargata un nucleo attorniato da alcuni organuli; al centro un mitocondrio; all'estremità più sottile un cloroplasto rivestito da una membrana che risulta singola nelle sezioni da noi osservate. La cellula è rivestita da una sottile parete e sembra non possedere vacuolo. La divisione cellulare inizia all'estremità distale del cloroplasto, interessa successivamente il mitocondrio, e termina con il nucleo. Tale alga non è mai stata segnalata finora; gli autori ritengono che le sue peculiarità siano tali da permettere l'istituzione su di essa di un nuovo genere Cyanidioschyzon e di una nuova specie e le assegnano pertanto il binomio Cyanidioschyzon merolae.
We determined the complete nucleotide sequence of the plastid genome of the unicellular marine red alga Porphyridium purpureum strain NIES 2140, belonging to the unsequenced class Porphyridiophyceae. The genome is a circular DNA composed of 217,694 bp with the GC content of 30.3 %. Twenty-nine of the 224 protein-coding genes contain one or multiple intron(s). A group I intron was found in the rpl28 gene, whereas the other introns were group II introns. The P. purpureum plastid genome has one non-coding RNA (ncRNA) gene, 29 tRNA genes and two nonidentical ribosomal RNA operons. One rRNA operon has a tRNA(Ala)(UGC) gene between the rrs and the rrl genes, whereas another has a tRNA(Ile)(GAU) gene. Phylogenetic analyses suggest that the plastids of Heterokontophyta, Cryptophyta and Haptophyta originated from the subphylum Rhodophytina. The order of the genes in the ribosomal protein cluster of the P. purpureum plastid genome differs from that of other Rhodophyta and Chromalveolata. These results suggest that a large-scale rearrangement occurred in the plastid genome of P. purpureum after its separation from other Rhodophyta.
Gracilaria chilensis sp.nov. is described and recorded from 30° S to 42° S on the coast of Chile. It closely resembles G. lemaneiformis (Bory) Weber-van Bosse, which also occurs in this region, and has been known by both this name and G. verrucosa (Hudson) Papenfuss. Gracilaria chilensis differs fundamentally from these species in having spermatangia in deep cortical (textorii-type) conceptacles and in having basal absorbing filaments in the cystocarp. Isolates of the species from sites 1300 km apart were cultured through the complete life history and used to verify conspecificity of reproductive plants in field collections. Moreover, the isolates were interfertile, thus demonstrating genetic compatibility of widely disjunct populations and verifying the distribution range. Because of its wide thermal and halotolerance, it is suggested that G. chilensis is distributed farther north and south in the eastern Pacific than present records indicate.
Plastids (chloroplasts) have long been recognized to have originated by endosymbiosis of a cyanobacterium, but their subsequent evolutionary history has proved complex because they have also moved between eukaryotes during additional rounds of secondary and tertiary endosymbioses. Much of this history has been revealed by genomic analyses, but some debates remain unresolved, in particular those relating to secondary red plastids of the chromalveolates, especially cryptomonads. Here, I examine several fundamental questions and assumptions about endosymbiosis and plastid evolution, including the number of endosymbiotic events needed to explain plastid diversity, whether the genetic contribution of the endosymbionts to the host genome goes far beyond plastid-targeted genes, and whether organelle origins are best viewed as a singular transition involving one symbiont or as a gradual transition involving a long line of transient food/symbionts. I also discuss a possible link between transporters and the evolution of protein targeting in organelle integration. Expected final online publication date for the Annual Review of Plant Biology Volume 64 is April 29, 2013. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
The chloroplast genomes of two photosynthetic euglenoids, Colacium vesiculosum Ehrenberg (128,889 bp), and Strombomonas acuminata (Schmarda) Deflandre (144,167 bp) have been sequenced. These chloroplast genomes in combination with those of Euglena gracilis, Eutreptia viridis, and Eutreptiella gymnastica provide a snapshot of euglenoid chloroplast evolution allowing comparisons of gene content, arrangement, and expansion. The gene content of the five chloroplast genomes is very similar varying only in the presence or absence of, rrn5, roaA, psaI, psaM, rpoA, and two tRNAs. Large gene rearrangements have occurred within the C. vesiculosum and S. acuminata chloroplast genomes. Most of these rearrangements represent repositioning of entire operons rather than single genes. When compared with previously sequenced genomes, C. vesiculosum and S. acuminata chloroplast genomes more closely resemble the E. gracilis chloroplast genome in size of the genome, number of introns, and gene order than they do those of the Eutreptiales. Overall, the chloroplast genomes of these five species show an evolutionary trend toward increased intron number, a decrease in gene density, and substantial rearrangement of gene clusters.
A novel unicellular red alga collected from a mangrove area on Iriomote Island in southwest Japan is described
as Bulboplastis apyrenoidosa gen. et sp. nov. The cells are spherical, mean 11.2 mm in diameter, and surrounded by a thick mucilaginous sheath. The grayishgreen chloroplast has many lobes extending throughout the cell and lacks a pyrenoid. This chloroplast type is similar to Glaucosphaera vacuolata, but differs from other unicellular red algae. Plastoglobuli clusters occur beneath the chloroplast envelope but only at the cell
periphery. A peripheral encircling thylakoid is absent.
Golgi bodies surround the central nucleus, which is an
arrangement shared with all members of the Dixoniellales. The subcellular features of some mitotic phases
are quite similar to those of other unicellular red algae. A pair of ring-shaped structures located within electrondense material can be seen in cells undergoing telophase. The size of the polar rings ranged within those reported from the Dixoniellales. A phylogenetic analysis based on small subunit rDNA indicates that B. apyrenoidosa is a member of the Dixoniellales and a sister lineage to Neorhodellaand Dixoniella.
SUMMARYA new unicellular red alga, Corynoplastis japonica gen. et sp. nov., is described from Tobishima, Japan. Cells are spherical, 18–33 µm in diameter, pale purple to brownish red and surrounded by a mucilaginous sheath. A single chloroplast with many lobes extends from the cell periphery to the cell center. A peripheral thylakoid is present. A pyrenoid occurs at each innermost chloroplast lobe end and one or two thylakoids are present in the pyrenoid matrix. The nucleus is eccentric to peripheral and Golgi bodies are scattered throughout the cell and associated with endoplasmic reticulum. Cells have a slow random gliding motility. The low molecular weight carbohydrate mannitol is present in the cells. Molecular phylogenetic analysis indicates that this alga is closely related to members of the genus Rhodella. A new order, Dixoniellales, is established for Dixoniella, Neorhodella and Glaucosphaera based on molecular and ultrastructural evidence (Golgi bodies associated only with the nucleus). The redefined order Rhodellales in which Rhodella and Corynoplastis are placed is characterized ultrastructurally by Golgi bodies scattered throughout the cytoplasm and associated with endoplasmic reticulum.
Phylogenetic comparisons suggest that plastid primary endosymbiosis, in which a single-celled protist engulfs and ‘enslaves’ a cyanobacterium, likely occurred once and resulted in the primordial alga. This photosynthetic cell diversified, through vertical evolution, into the ubiquitous green (Chlorophyta) and red (Rhodophyta) algae, and the more scarce Glaucophyta. However, some modern algal lineages have a more complicated evolutionary history involving a secondary endosymbiotic event, in which a protist engulfed an existing eukaryotic alga (rather than a cyanobacterium), which was then reduced to a secondary plastid. Secondary endosymbiosis explains the majority of algal biodiversity, yet the number and timing of these events is unresolved. Here we analyzed a five-gene plastid dataset to show that a diverse group of chlorophyll c-containing protists comprising cryptophyte, haptophyte, and stramenopiles algae (Chromista) share a common plastid that most likely arose from a single, ancient (about 1260 million years ago) secondary endosymbiosis involving a red alga. This finding is consistent with C. monophyly and implicates secondary endosymbiosis as a driving force in early eukaryotic evolution.
Plastids, the light-harvesting organelles of plants and algae, are the descendants of cyanobacterial endosymbionts that became
permanent fixtures inside nonphotosynthetic eukaryotic host cells. This chapter provides an overview of the structural, functional
and molecular diversity of plastids in the context of current views on the evolutionary relationships among the eukaryotic
hosts in which they reside. Green algae, land plants, red algae and glaucophyte algae harbor double-membrane-bound plastids
whose ancestry is generally believed to trace directly to the original cyanobacterial endosymbiont. In contrast, the plastids
of many other algae, such as dinoflagellates, diatoms and euglenids, are usually bound by more than two membranes, suggesting
that these were acquired indirectly via endosymbiotic mergers between nonphotosynthetic eukaryotic hosts and eukaryotic algal
endosymbionts. An increasing amount of genomic data from diverse photosynthetic taxa has made it possible to test specific
hypotheses about the evolution of photosynthesis in eukaryotes and, consequently, improve our understanding of the genomic
and biochemical diversity of modern-day eukaryotic phototrophs.
A comprehensive assessment of the origin and evolution of plastids will require more information on the nature of plastid genomes from non-green algae. I have constructed a physical map of the chloroplast genome from the red alga Porphyra yezoensis. The 185 kb circular genome contains ribosomal RNA encoding inverted repeats (6.6 kb), and is divided into small and large singlecopy regions of approxiamtely 16 kb and 156 kb respectively. The Porphyra genome contains several genes not found in higher plant chloroplasts. Genes encoding the pigmented, light-harvesting phycobiliproteins are organized relatively close to one another on the genome, and represent components of a multi-gene family. the phycocyanin biliprotein genes (ppcBA) map in two single-copy regions, suggesting either duplicated genes or a transsplicing mechanism. In contrast to higher plants, the tufA and rbcS genes are chloroplast-encoded in Porphyra, and rbcS is clustered with the rbcL gene, suggesting an operon type of arrangement. The Porphyra chloroplast genome is distinctive, also, in that part of it has sequence homology to plasmid-like DNA molecules which co-isolate with the chloroplast DNA.
Plasmids from extant plants exhibit considerable diversity in morphological and biochemical characters. Although most authors have agreed on xenogenous (endosymbiotic) rather than autogenous origins of plastids (discussed by Doolittle (1982) in ‘The Biology of Cyanobacteria’), details concerning the endosymbiotic events remain unresolved.
In the eleven years since ‘The Biology of Cyanobacteria’, many data have accumulated that, while supporting the xenogenous origin of plastids, have revived the controversy over single (monophyletic) versus multiple (polyphyletic) origins. These arguments revolve around the number and nature of the primary endosymbiont(s) that gave rise to the first plastid-bearing eucaryotes. The question of whether secondary endosymbiotic events, originally hypothesized on the basis of electron microscopic evidence, were responsible for the formation of ‘complex’ plastids (those surrounded by more than two membranes) has now been investigated by molecular methods.
The purpose of this chapter is to present recent evidence bearing on the probable nature of the procaryotic ancestor(s) involved in the primary endosymbiotic event(s), and on the secondary endosymbiotic events that gave rise to eucaryotes bearing complex plastids. Comparisons of gene content, gene arrangement, gene expression and gene sequences between extant cyanobacteria and plastids give important clues about the possible ancestors of plastids and of the subsequent transformation of a eubacterial genome into a plastid genome. In the last several years, four complete land plant plastid genomes have been sequenced, contributing vastly to our knowledge of plastid architecture and expression. In addition, a great deal of molecular data has been acquired on cyanelle and cyanobacterial genes and genomes. Increased emphasis has now been placed on the study of non-land plant plastid genomes and a number of rhodophyte, chromophyte, cryptophyte and euglenophyte plastid genomes have been extensively mapped and sequenced. These data are presented and the phylogenetic implications evaluated.
The wondrously diverse eukaryotes that constitute the red algae have been the focus of numerous recent molecular surveys and remain a rich source of undescribed and little known species for the traditional taxonomist. Molecular studies place the red algae in the kingdom Plantae; however, supraordinal classification has been largely confined to debate on subclass vs. class level status for the two recognized subgroups, one of which is widely acknowledged as paraphyletic. This narrow focus has generally masked the extent to which red algal classification needs modification. We provide a comprehensive review of the literature pertaining to the antiquity, diversity, and systematics of the red algae and propose a contemporary classification based on recent and traditional evidence.