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Domain structure of several different types of genomic loci including proteins that contain DUF1501, PSCyt1/2, and PSD1 domains in the Verrucomicrobium spinosum genome. Evolutionary relationships between several DUF1501 domain-containing proteins from the V. spinosum genome, representing genomic loci of different architecture conserved across several species, are shown. GI numbers of corresponding V. spinosum proteins are used as tip labels. Forward and reverse orientation in the genome are denoted by F or R sign. Domain architecture is shown for the genomic neighborhood of every DUF1501 domain-containing protein. Codes for the different domains are shown in the figure inset. Large-scale phylogeny for all DUF1501-containing proteins identified in all completely sequenced bacterial genomes, and complete or draft PVC genomes, is shown in supplementary figure S13, Supplementary Material online.
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The Planctomycetes, Verrucomicrobia, Chlamydiae (PVC) super-phylum contains bacteria with either complex cellular organization or simple cell structure; it also includes organisms of different lifestyles (pathogens, mutualists, commensal, and free-living). Genome content evolution of this group has not been studied in a systematic fashion, which wo...
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... included all gene families containing two or more se- quences in the genome flux analysis and used loss and speci- ation costs fixed at 1.0 and 0.0, respectively. Minimal genome flux was obtained with HGT penalty equal to 5, and duplica- tion penalty equal to 3 (supplementary fig. S4, Supplementary Material ...Context 2
... proteins most strongly associated with DUF1501 featured a cytochrome c motif con- taining domains PSCyt1 and PSCyt2 (PF07635 and PF07583) and domain of unknown function PSD1 (PF07587), previously identified to be specific for R. baltica ( Studholme et al. 2004). Figure 4 shows the domain composition of several genomic clusters containing DUF1501 proteins found in the genome of V. spinosum, present in a variety of other PVC species and showing clear grouping within the phylogenetic tree of DUF1501-containing proteins (supplementary fig. S14, Sup- plementary Material online). ...Citations
... The first group consisted of the Candidate phylum Bipolaricaulota, characterized by its deep branching within the bacterial domain and the presence of members capable of autotrophic carbon fixation via the ancient Wood-Ljungdahl pathway for carbon fixation (Takami et al., 2012). We further explored the superphylum Planctomycetes, Verrucomicrobia, Chlamydiae (PVC), which encompasses bacteria exhibiting eukaryote-like cellular compartmentalization and varying degrees of cell organization (Kamneva et al., 2012). Lastly, we focused on Cyanobacteria, due to their pivotal role as primary producers in the microbial ecosystem, influencing carbon and nitrogen cycles (Elster and Kvíderová, 2011). ...
A comprehensive study was conducted in the Cuatro Ciénegas Basin (CCB) in Coahuila, Mexico, which is known for its diversity of microorganisms and unique physicochemical properties. The study focused on the “Archaean Domes” (AD) site in the CCB, which is characterized by an abundance of hypersaline, non-lithifying microbial mats. In AD, we analyzed the small domes and circular structures using metagenome assembly genomes (MAGs) with the aim of expanding our understanding of the prokaryotic tree of life by uncovering previously unreported lineages, as well as analyzing the diversity of bacteria and archaea in the CCB. A total of 325 MAGs were identified, including 48 Archaea and 277 Bacteria. Remarkably, 22 archaea and 104 bacteria could not be classified even at the genus level, highlighting the remarkable novel diversity of the CCB. Besides, AD site exhibited significant diversity at the phylum level, with Proteobacteria being the most abundant, followed by Desulfobacteria, Spirochaetes, Bacteroidetes, Nanoarchaeota, Halobacteriota, Cyanobacteria, Planctomycetota, Verrucomicrobiota, Actinomycetes and Chloroflexi. In Archaea, the monophyletic groups of MAGs belonged to the Archaeoglobi, Aenigmarchaeota, Candidate Nanoarchaeota, and Halobacteriota. Among Bacteria, monophyletic groups were also identified, including Spirochaetes, Proteobacteria, Planctomycetes, Actinobacteria, Verrucomicrobia, Bacteroidetes, Candidate Bipolaricaulota, Desulfobacteria, and Cyanobacteria. These monophyletic groups were possibly influenced by geographic isolation, as well as the extreme and fluctuating environmental conditions in the pond AD, such as stoichiometric imbalance of C:N:P of 122:42:1, fluctuating pH (5–9.8) and high salinity (5.28% to saturation).
... Despite contrasting genomic features, all described chlamydiae share a biphasic lifestyle with an intracellular replicative phase as reticulate bodies (RBs) and a nondividing extracellular phase as elementary bodies (EBs) 19 . Chlamydiae diverged from other PVC bacteria 1-2 billion years ago (Ga) 29,30 , and their endosymbiotic lifestyle is proposed to have evolved early 29,[31][32][33] . It was also thought that the chlamydial ancestor resembled extant protist-infecting lineages and had greater coding potential and metabolic versatility while other chlamydial groups underwent genome reduction. ...
... Despite contrasting genomic features, all described chlamydiae share a biphasic lifestyle with an intracellular replicative phase as reticulate bodies (RBs) and a nondividing extracellular phase as elementary bodies (EBs) 19 . Chlamydiae diverged from other PVC bacteria 1-2 billion years ago (Ga) 29,30 , and their endosymbiotic lifestyle is proposed to have evolved early 29,[31][32][33] . It was also thought that the chlamydial ancestor resembled extant protist-infecting lineages and had greater coding potential and metabolic versatility while other chlamydial groups underwent genome reduction. ...
... Furthermore, we have shown that key genes were gained before LVCCA, and that LCCA also evolved through a reduction in pathways involved in de novo biosynthesis and hence a dependence on uptake of essential metabolites. Chlamydiae diverged from other PVC bacteria between 1 and 2 Ga, coinciding with estimates for the evolution of eukaryotes (1.2-2.1 Ga) 29,30,32,33 . Our reconstruction demonstrates that LCCA was already an obligate endosymbiont, indicating a billion-year-old history of chlamydiae infecting eukaryotic hosts as they evolved. ...
Chlamydiae is a bacterial phylum composed of obligate animal and protist endosymbionts. However, other members of the Planctomycetes–Verrucomicrobia–Chlamydiae superphylum are primarily free living. How Chlamydiae transitioned to an endosymbiotic lifestyle is still largely unresolved. Here we reconstructed Planctomycetes–Verrucomicrobia–Chlamydiae species relationships and modelled superphylum genome evolution. Gene content reconstruction from 11,996 gene families suggests a motile and facultatively anaerobic last common Chlamydiae ancestor that had already gained characteristic endosymbiont genes. Counter to expectations for genome streamlining in strict endosymbionts, we detected substantial gene gain within Chlamydiae. We found that divergence in energy metabolism and aerobiosis observed in extant lineages emerged later during chlamydial evolution. In particular, metabolic and aerobic genes characteristic of the more metabolically versatile protist-infecting chlamydiae were gained, such as respiratory chain complexes. Our results show that metabolic complexity can increase during endosymbiont evolution, adding an additional perspective for understanding symbiont evolutionary trajectories across the tree of life.
... Functional metagenomic evidence led to the identification of 60 genes of mucin degradation and a salt-tolerant gene in A. muciniphila (Culligan et al., 2012;Kamneva et al., 2012). A. muciniphila can grow in a culture medium with bile extract and the presence of 0.1 % bile salts, but it cannot tolerate 0.5 % pure bile salts (van der Ark et al., 2017;van der Ark, 2018). ...
Numerous studies have almost proven the beneficial effects of gut microbiota in various aspects of human health, and even the gut microbiota is known as a new and forgotten organ. Akkermansia muciniphila, as a member of the gut microbiota, is considered a bacterium with probiotic properties; consequently, it has a remarkable position in microbiome research. This bacterium accounts for about 1–4 % of the total fecal microbiota population and is also considered a health marker. The accumulated evidence has shown a significant association between A. muciniphila and several disorders and diseases, such as obesity, fatty liver disease, diabetes, and even behavioral disorders. On the other hand, the beneficial effects of A. muciniphila in different studies have shown, such as protective role against pathogenic agents, antitumor properties, tight junctions’ improvement, reduction of inflammation, gut permeability, and boosting adaptive immune responses. In this review, based on the available evidence and the latest research, we comprehensively evaluated the impact of A. muciniphila on host health from three points of view: metabolic, protective, and immune functions, as well as the possible mechanisms of each process.
... To obtain insights into gene family dynamics, we reconciled every gene tree with the species tree using AnGST [32]. Gene-tree species-tree reconciliation may help us to explicitly infer the evolutionary history of every gene family in the dataset [33]. The evolutionary history usually includes gene birth, duplication, loss, and horizontal gene transfer (HGT) events. ...
Erysipelothrix rhusiopathiae is a causative agent of erysipelas in animals and erysipeloid in humans. However, current information regarding E. rhusiopathiae pathogenesis remains limited. Previously, we identified two E. rhusiopathiae strains, SE38 and G4T10, which were virulent and avirulent in pigs, respectively. Here, to further study the pathogenic mechanism of E. rhusiopathiae, we sequenced and assembled the genomes of strains SE38 and G4T10, and performed a comparative genomic analysis to identify differences or mutations in virulence-associated genes. Next, we comparatively analyzed 25 E. rhusiopathiae virulence-associated genes in SE38 and G4T10. Compared with that of SE38, the spaA gene of the G4T10 strain lacked 120 bp, encoding repeat units at the C-terminal of SpaA. To examine whether these deletions or splits influence E. rhusiopathiae virulence, these 120 bp were successfully deleted from the spaA gene in strain SE38 by homologous recombination. The mutant strain ΔspaA displayed attenuated virulence in mice and decreased adhesion to porcine iliac artery endothelial cells, which was also observed using the corresponding mutant protein SpaA’. Our results demonstrate that SpaA-mediated adhesion between E. rhusiopathiae and host cells is dependent on its C-terminal repeat units.
... C hlamydiae forms with Planctomycetes and Verrucomicrobia phyla a very ancient monophyletic group of bacteria known as PVC, which has been recently enriched with additional phyla 1 . The Chlamydiales consists of members of the Chlamydiaceae family that includes etiological agents of human and animal infectious diseases and at of least eight additional families commonly named "chlamydia-related bacteria" or "environmental" chlamydia 2,3 . ...
The order Chlamydiales includes obligate intracellular pathogens capable of infecting mammals, fishes and amoeba. Unlike other intracellular bacteria for which intracellular adaptation led to the loss of glycogen metabolism pathway, all chlamydial families maintained the nucleotide-sugar dependent glycogen metabolism pathway i.e. the GlgC-pathway with the notable exception of both Criblamydiaceae and Waddliaceae families. Through detailed genome analysis and biochemical investigations, we have shown that genome rearrangement events have resulted in a defective GlgC-pathway and more importantly we have evidenced a distinct trehalose-dependent GlgE-pathway in both Criblamydiaceae and Waddliaceae families. Altogether, this study strongly indicates that the glycogen metabolism is retained in all Chlamydiales without exception, highlighting the pivotal function of storage polysaccharides, which has been underestimated to date. We propose that glycogen degradation is a mandatory process for fueling essential metabolic pathways that ensure the survival and virulence of extracellular forms i.e. elementary bodies of Chlamydiales.
... 22 To investigate the association of bacteria with plasmids over an extended evolutionary time period, we chose the Chlamydiae, a phylum of obligate intracellular pathogens and symbionts that have engaged in a host-associated lifestyle around a billion years ago. [23][24][25] A strictly host dependent lifestyle has severe evolutionary consequences for bacterial genomes. Due to small population sizes, genetic drift, and limited access to large gene pools, endosymbiont genomes accumulate deleterious mutations eventually leading to genome size reduction. ...
... The monophyly of the phylum chlamydiae and its major families is well supported by phylogenomic analysis in previous studies 24,50,53 and confirmed with our comprehensive dataset comprising high-quality genomes of plasmid-containing and plasmid-less chlamydiae ( Figure S1; Data S1). First, we compared the chlamydial plasmids in our dataset to known plasmids from other bacterial phyla and found that their size of 7.5-145 kb falls into the range of described bacterial plasmids (Figure S2A). ...
... The reconstructed ancestral plasmid last common ancestor (plasmid LCA or pLCA) present in the LCA of all chlamydiae contained 11 plasmid gene families ( Figure 6; Table S2), including parA/pgp5, the helicase pgp1, and pgp6, the two latter of which are essential for the maintenance of extant Chlamydiaceae plasmids. 57 Molecular dating of the chlamydiae LCA estimated an age of 700 My to one billion years, 23,24 which likely places the chlamydiae pLCA at approximately the same time. ...
Plasmids are important in microbial evolution and adaptation to new environments. Yet, carrying a plasmid
can be costly, and long-term association of plasmids with their hosts is poorly understood. Here, we provide
evidence that the Chlamydiae, a phylum of strictly host-associated intracellular bacteria, have coevolved with
their plasmids since their last common ancestor. Current chlamydial plasmids are amalgamations of at least
one ancestral plasmid and a bacteriophage. We show that the majority of plasmid genes are also found on
chromosomes of extant chlamydiae. The most conserved plasmid gene families are predominantly vertically
inherited, while accessory plasmid gene families show significantly increased mobility. We reconstructed the
evolutionary history of plasmid gene content of an entire bacterial phylum over a period of around one billion
years. Frequent horizontal gene transfer and chromosomal integration events illustrate the pronounced
impact of coevolution with these extrachromosomal elements on bacterial genome dynamics in host-dependent microbes.
... The Ancient Origin of the Intracellular Lifestyle of Chlamydiae The well-conserved basic features of known chlamydiae, phylogenetic and phylogenomic analysis suggest that the last common ancestor of all chlamydiae had already adopted an intracellular lifestyle 1-2 billion years ago [75][76][77]. Consistent with this notion, an interesting hypothesis suggested ancient chlamydiae as facilitators of the evolution of the first photosynthetic eukaryotes (Box 2). ...
... The addition of more genomes from deep-branching lineages reduced the chlamydial core genome, whereas the accessory genome expanded strongly. The application of different techniques and data sets led to differences in numbers of core genes proposed for chlamydiae [20,21,63,76,79]. After including the smallest genomes of the fish-pathogenic Parilichlamydiaceae, the chlamydial core genome included around 340 genes (11-49% of all protein-coding sequences per genome) [21]. ...
... The small genomes of Parilichlamydiaceae lack signs of any recent HGT [21], supporting the view that HGT played only a minor part during evolution of chlamydiae residing in vertebrate hosts [76,91]. Chlamydiae associated with arthropods and protists, however, encode a much higher percentage of genes acquired by HGT [78,91,92]. ...
Chlamydiae have been known for more than a century as major pathogens of humans. Yet they are also found ubiquitously in the environment where they thrive within protists and in an unmatched wide range of animals. This review summarizes recent advances in understanding chlamydial diversity and distribution in nature. Studying these environmental chlamydiae provides a novel perspective on basic chlamydial biology and evolution. A picture is beginning to emerge with chlamydiae representing one of the evolutionarily most ancient and successful groups of obligate intracellular bacteria.
... Specifically, it has been shown that Planctopirus limnophilus is able to import fluorescent dextran under laboratory conditions (Boedeker et al. 2017). Although the uptake mechanisms remain to be determined, clathrin-like membrane-coat proteins associated with vesicles have been identified that are analogous to the eukaryotic membranecoat proteins involved in endocytosis (Santarella-Mellwig et al. 2010;Kamneva et al. 2012). Furthermore, studies performed in G. obscuriglobus has shown that transcription is spatially segregated from translation (Gottshall et al. 2014) and that the nucleoid is highly condensed (Yee et al. 2012). ...
... Previous comparative genomic studies of cultivated representatives from the so-called PVC superphylum, which includes Planctomycetes, Verrucomicrobia, and Chlamydiae, have identified candidate genes of unknown functions potentially associated with the complex cell plan (Kamneva et al. 2012). The analyses also indicated elevated rates of duplications and horizontal gene transfers in the lineage leading to G. obscuriglobus (Kamneva et al. 2012). ...
... Previous comparative genomic studies of cultivated representatives from the so-called PVC superphylum, which includes Planctomycetes, Verrucomicrobia, and Chlamydiae, have identified candidate genes of unknown functions potentially associated with the complex cell plan (Kamneva et al. 2012). The analyses also indicated elevated rates of duplications and horizontal gene transfers in the lineage leading to G. obscuriglobus (Kamneva et al. 2012). Overall, 2,840 genes of the 7,989 genes in total in G. obscuriglobus were inferred to be part of multigene families in this lineage (Kamneva et al. 2012). ...
Bacteria of the phylum Planctomycetes have a unique cell plan with an elaborate intracellular membrane system, thereby resembling eukaryotic cells. The origin and evolution of these remarkable features is debated. To study the evolutionary genomics of bacteria with complex cell architectures, we have re-sequenced the 9.2 Mb genome of the model organism Gemmata obscuriglobus and sequenced the 10 Mb genome of Gemmata massiliana Soil9, the 7.9 Mb genome of Cjuql4 and the 6.7 Mb genome of Tuwongella immobilis, all of which belong to the family Gemmataceae. A gene flux analysis of the Planctomycetes revealed a massive emergence of novel protein families at multiple nodes within the Gemmataceae. The expanded protein families have unique multi-domain architectures composed of domains that are characteristic of prokaryotes, such as the sigma factor domain of extracytoplasmic sigma factors, and domains that have proliferated in eukaryotes, such as the WD40, LRR, TPR and Ser/Thr kinase domains. Proteins with identifiable domains in the Gemmataceae have longer lengths and linkers than proteins in most other bacteria, and the analyses suggest that these traits were ancestrally present in the Planctomycetales. A broad comparison of protein length distribution profiles revealed an overlap between the longest proteins in prokaryotes and the shortest proteins in eukaryotes. We conclude that the many similarities between proteins in the Planctomycetales and the eukaryotes are due to convergent evolution and that there is no strict boundary between prokaryotes and eukaryotes with regard to features such as gene paralogy, protein length and protein domain composition patterns.
... As shown by our data (Fig 3), bacteria of the phyla Chlamydiae and Verrucomicrobia mainly contain six S1 domains, while Planctomycetes can have four, five, and six S1 domains. According to some published data, the genome of organisms of the phylum Planctomycetes compared with other phyla of superphylum PVC is the largest and most susceptible to evolutionary changes [26]. ...
The family of ribosomal proteins S1 contains about 20% of all bacterial proteins including the S1 domain. An important feature of this family is multiple copies of structural domains in bacteria, the number of which changes in a strictly limited range from one to six. In this study, the automated exhaustive analysis of 1453 sequences of S1 allowed us to demonstrate that the number of domains in S1 is a distinctive characteristic for phylogenetic bacterial grouping in main phyla. 1453 sequences of S1 were identified in 25 out of 30 different phyla according to the List of Prokaryotic Names with Standing in Nomenclature. About 62% of all records are identified as six-domain S1 proteins, which belong to phylum Proteobacteria. Four-domain S1 are identified mainly in proteins from phylum Firmicutes and Actinobacteria. Records belonging to these phyla are 33% of all records. The least represented two-domain S1 are about 0.6% of all records. The third and fourth domains for the most representative four- and six-domain S1 have the highest percentage of identity with the S1 domain from polynucleotide phosphorylase and S1 domains from one-domain S1. In addition, for these groups, the central part of S1 (the third domain) is more conserved than the terminal domains.
... Potential applications of such studies are widespread and affecting a vast variety of fundamental biological research areas such as molecular biology, microbiology, and biotechnology [19]. For example, evolutionary histories of gene duplications provide a comprehensive way to describe the dynamics of gene family evolution [9,18] and are also a popular tool to differentiate between orthologous and paralogous genes [1,2], a primary task in the functional determination of genes [17]. ...
... Gene families play a significant role in the systematic analysis of protein function, diversity of multicellular organisms, and related areas [4,16,18]. Therefore, categorizing genes into credible families is an ongoing and central topic in phylogenetics. Recently, as part of this effort, the classic gene duplication model has been augmented by incorporating the knowledge of whole genome duplications [22]. ...
Gene duplications are a dominant force in creating genetic novelty, and studying their evolutionary history is benefiting various research areas. The gene duplication model, which was introduced more than 40 years ago, is widely used to infer duplication histories by resolving the discordance between the evolutionary history of a gene family and the species tree through which this family has evolved. Today, for many gene families lower bounds on the number of gene duplications that have occurred along each edge of the species tree, called duplication scenarios, can be derived, for example from genome duplications. Recently, the gene duplication model has been augmented to include duplication scenarios and to address the question of whether such a scenario is feasible for a given gene family. Non-feasibility of a duplication scenario for a gene family can provide a strong indication that this family might not be well-resolved, and identifying well-resolved gene families is a challenging task in evolutionary biology. However, genome duplications are often followed by episodes of gene losses, and lost genes can explain non-feasible duplication scenarios. Here, we address this major shortcoming of the augmented duplication model, by proposing a gene duplication model that incorporates duplication-loss scenarios. We describe efficient algorithms that decide whether a duplication-loss scenario is feasible for a gene family; and if so, compute a gene tree for the family that infers the minimum duplication-loss events satisfying the scenario.
