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Composition of fungi within H. obscurata. (A) Proportion of total fungal ASVs assigned to taxonomic rank; (B) Relative abundance of fungi within H. obscurata at the genus level for each sample; (C ˗ E) Average relative abundance of endolichenic fungal communities in H. obscurata at the class (C), order (D) and family (E) levels; (F) Relative abundance of endolichenic fungi in H. obscurata at the genus level for each sample
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The dual nature of fungal-algal lichen symbioses is extended by other microbial associations. Increasing evidence has confirmed that lichens are successful holobionts composed of complex and multiple species. Specific interactions between these microbes contributed to the lichens’ health, growth and fitness. Previous studies suggested that the comp...
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... edu/ galaxy/; accessed on 14 July 2023) [37,38]. While previous investigations of lichen-associated bacteria commonly established a default threshold LDA score of 2 [39,40], this study adopted threshold scores of 3 and 4 to concentrate the analysis on significant differences observed in substantial statistical indicators between the two distinct sampling regions. Indicators exhibiting an LDA score exceeding 4 underwent additional scrutiny to assess differential abundances between the two regions, which was carried out using the Analysis of Compositions of Microbiomes with Bias Correction (ANCOM-BC) methodology [41]. ...
The diversity of bacteria associated with alpine lichens was profiled. Lichen samples belonging to the Umbilicariaceae family, commonly known as rock tripe lichens, were gathered from two distinct alpine fellfields: one situated on Mt. Brennkogel located in the Eastern European Alps (Austria), and the other on Mt. Stanley located in the Rwenzori mountains of equatorial Africa (Uganda). The primary aim of this research was to undertake a comparative investigation into the bacterial compositions, and diversities, identifying potential indicators and exploring their potential metabolisms, of these lichen samples. Bulk genomic DNA was extracted from the lichen samples, which was used to amplify the 18S rRNA gene by Sanger sequencing and the V3-V4 region of the 16S rRNA gene by Illumina Miseq sequencing. Examination of the fungal partner was carried out through the analysis of 18S rRNA gene sequences, belonging to the genus Umbilicaria (Ascomycota), and the algal partner affiliated with the lineage Trebouxia (Chlorophyta), constituted the symbiotic components. Analyzing the MiSeq datasets by using bioinformatics methods, operational taxonomic units (OTUs) were established based on a predetermined similarity threshold for the V3-V4 sequences, which were assigned to a total of 26 bacterial phyla that were found in both areas. Eight of the 26 phyla, i.e. Acidobacteriota, Actinomycota, Armatimonadota, Bacteroidota, Chloroflexota, Deinococcota, Planctomycetota, and Pseudomonadota, were consistently present in all samples, each accounting for more than 1% of the total read count. Distinct differences in bacterial composition emerged between lichen samples from Austria and Uganda, with the OTU frequency-based regional indicator phyla, Pseudomonadota and Armatimonadota, respectively. Despite the considerable geographic separation of approximately 5430 km between the two regions, the prediction of potential metabolic pathways based on OTU analysis revealed similar relative abundances. This similarity is possibly influenced by comparable alpine climatic conditions prevailing in both areas.
... Hemichloris as Cladonia photobionts is uncertain. Hemichloris antarctica is considered part of the cryptoendolithic microbial community [106,107], and although it has been found in lichen thalli of various species in low proportion [98,108,109], most authors do not consider this species to be a possible photobiont. Similarly, the ASV of Coccomyxa accounts for less than 1% of the total reads. ...
This study explores the diversity of photobionts associated with the Mediterranean lichen-forming fungus Cladonia subturgida. For this purpose, we sequenced the whole ITS rDNA region by Sanger using a metabarcoding method for ITS2. A total of 41 specimens from Greece, Italy, France, Portugal, and Spain were studied. Additionally, two specimens from Spain were used to generate four cultures. Our molecular studies showed that the genus Myrmecia is the main photobiont of C. subturgida throughout its geographic distribution. This result contrasts with previous studies, which indicated that the main photobiont for most Cladonia species is Asterochloris. The identity of Myrmecia was also confirmed by ultrastructural studies of photobionts within the lichen thalli and cultures. Photobiont cells showed a parietal chloroplast lacking a pyrenoid, which characterizes the species in this genus. Phylogenetic analyses indicate hidden diversity within this genus. The results of amplicon sequencing showed the presence of multiple ASVs in 58.3% of the specimens studied.
... Here, we present evidence that green alga Coccomyxa viridis is widespread in lichens as a minor component present in addition to the main photobiont. C. viridis has been reported before from lichens with various non-Coccomyxa photobionts in several isolated reports 13,14,16,20,21,31 . Species from the C. viridis clade have been independently cultured from several lichen symbioses 13,14,16 . ...
... Species from the C. viridis clade have been independently cultured from several lichen symbioses 13,14,16 . In addition, several amplicon metabarcoding studies of lichen algae reported small numbers of reads assigned to C. viridis 20,21,31 . Now, these reports are confirmed by our systematic screening of lichen metagenomic data. ...
Lichen symbiosis is centered around a relationship between a fungus and a photosynthetic microbe, usually a green alga. In addition to their main photosynthetic partner (the photobiont), lichen symbioses can contain additional algae present in low abundance. The biology of these algae and the way they interact with the rest of lichen symbionts remains largely unknown. Here we present the first genome sequence of a non-photobiont lichen-associated alga. Coccomyxa viridis was unexpectedly found in 12% of publicly available lichen metagenomes. With few exceptions, members of the Coccomyxa viridis clade occur in lichens as non-photobionts, potentially growing in thalli endophytically. The 45.7 Mbp genome of C. viridis was assembled into 18 near chromosome-level contigs, making it one of the most contiguous genomic assemblies for any lichen-associated algae. Comparing the C. viridis genome to its close relatives revealed the presence of traits associated with the lichen lifestyle. The genome of C. viridis provides a new resource for exploring the evolution of the lichen symbiosis, and how symbiotic lifestyles shaped evolution in green algae.
... Hence, these fungi are ubiquitous in distribution and have been reported from various extreme and atypical environments, such as leaf surfaces [5,6], sub-aerial biofilms [7], human teeth [8], arctic landscapes [9], tropical oligotrophic peatlands [10], and pyramids [11]. Concurrently, various fungi from Teratosphaeriaceae have also been recovered from lichens [12,13]. ...
... Echoing the global trend, several novel endolichenic fungal taxa were also identified in China [24][25][26][27][28]. In a recent fungal biodiversity study by Xu et al. (2022), the authors detected a substantial diversity of endolichenic fungi in the family Teratosphaeriaceae from Heterodermia obscurata, and proposed that Teratosphaeriaceae is likely to be one of the core endophytic fungal families associated with this lichen [13]. The authors used a high-throughput sequencing platform; hence, no isolates could be retrieved. ...
... However, as of now, a few endolichenic fungi from Teratosphaeriaceae have been isolated from lichens [59], such as those from the genera Xanthoriicola and Austrostigmidium [12]. Contrarily, in a recent diversity study using a high throughput sequencing platform showed that Teratosphaeriaceae is the most abundant endolichenic fungal taxa associated with Heterodermia obscurata [13]. This contradiction is likely because a majority of endolichenic fungi are slow-growing, and in this regard, the isolates in this study are not an exception. ...
Fungi from the Teratosphaeriaceae (Mycosphaerellales; Dothideomycetes; Ascomycota) have a wide range of lifestyles. Among these are a few species that are endolichenic fungi. However, the known diversity of endolichenic fungi from Teratosphaeriaceae is far less understood compared to other lineages of Ascomycota. We conducted five surveys from 2020 to 2021 in Yunnan Province of China, to explore the biodiversity of endolichenic fungi. During these surveys, we collected multiple samples of 38 lichen species. We recovered a total of 205 fungal isolates representing 127 species from the medullary tissues of these lichens. Most of these isolates were from Ascomycota (118 species), and the remaining were from Basidiomycota (8 species) and Mucoromycota (1 species). These endolichenic fungi represented a wide variety of guilds, including saprophytes, plant pathogens, human pathogens, as well as entomopathogenic, endolichenic, and symbiotic fungi. Morphological and molecular data indicated that 16 of the 206 fungal isolates belonged to the family Teratosphaeriaceae. Among these were six isolates that had a low sequence similarity with any of the previously described species of Teratosphaeriaceae. For these six isolates, we amplified additional gene regions and conducted phylogenetic analyses. In both single gene and multi-gene phylogenetic analyses using ITS, LSU, SSU, RPB2, TEF1, ACT, and CAL data, these six isolates emerged as a monophyletic lineage within the family Teratosphaeriaceae and sister to a clade that included fungi from the genera Acidiella and Xenopenidiella. The analyses also indicated that these six isolates represented four species. Therefore, we established a new genus, Intumescentia gen. nov., to describe these species as Intumescentia ceratinae, I. tinctorum, I. pseudolivetorum, and I. vitii. These four species are the first endolichenic fungi representing Teratosphaeriaceae from China.
... accessed on 10 May 2022) [43]. While previous studies of lichen-associated microorganisms set the threshold LDA score to 2 [44,45], this study set the threshold to 4 and 5 in order to focus on biomarkers having large statistical differences between the two sampling regions. Differential abundance analysis was performed using the Analysis of Compositions of Microbiomes with Bias Correction (ANCOM-BC) [46]. ...
Increased research attention is being given to bacterial diversity associated with lichens. Rock tripe lichens (Umbilicariaceae) were collected from two distinct Antarctic biological regions, the continental region near the Japanese Antarctic station (Syowa Station) and the maritime Antarctic South Orkney Islands (Signy Island), in order to compare their bacterial floras and potential metabolism. Bulk DNA extracted from the lichen samples was used to amplify the 18S rRNA gene and the V3-V4 region of the 16S rRNA gene, whose amplicons were Sanger- and MiSeq-sequenced, respectively. The fungal and algal partners represented members of the ascomycete genus Umbilicaria and the green algal genus Trebouxia, based on 18S rRNA gene sequences. The V3-V4 sequences were grouped into operational taxonomic units (OTUs), which were assigned to eight bacterial phyla, Acidobacteriota, Actinomyceota, Armatimonadota, Bacteroidota, Cyanobacteria, Deinococcota, Pseudomonadota and the candidate phylum Saccharibacteria (also known as TM7), commonly present in all samples. The OTU floras of the two biological regions were clearly distinct, with regional biomarker genera, such as Mucilaginibacter and Gluconacetobacter, respectively. The OTU-based metabolism analysis predicted higher membrane transport activities in the maritime Antarctic OTUs, probably influenced by the sampling area’s warmer maritime climatic setting.
Lichen thalli host complex microbial communities, which may foster the ecological stability and longevity of the lichen symbiosis. Yet, we lack a holistic understanding of the processes contributing to the assembly of the lichen holobiont. This study assessed the diversity and community structure in taxonomically diverse co-occurring lichens associated with Trebouxiophyceae algae from Bolivian forests. We focused on three components of the lichen holobiont: the lichenized fungus (mycobiont) and its associated algae (photobiome) and fungi (mycobiome). We specifically tested the influence of mycobiont identity, thallus morphological type, reproductive strategy, and lichen secondary metabolites on the lichen-associated photobiome and mycobiome. To understand the specialization patterns between holobiont components, we investigated interaction networks.
We observed that co-occurring mycobiont taxa host diverse, taxon-specific, yet overlapping photobiome and mycobiome. In particular, these communities are significantly influenced by the host’s thallus morphological type and its secondary metabolites. Finally, we demonstrated that both photobiome and mycobiome are structured mainly by mycobiont identity, which results in modular networks with strong phylogenetic signals and high levels of specialization. In conclusion, the symbiotic interactions within lichen are structured mainly by the mycobiont, which appears to be the leading architect of the lichen holobiont.
Ten samples of tropical lichens collected from Doi Inthanon, Thailand, were explored for the diversity of their bacterial microbiomes through 16S rRNA-based metagenomics analysis. The five predominant lichen-associated bacteria belonged to the phyla Proteobacteria (31.84%), Planctomycetota (17.08%), Actinobacteriota (15.37%), Verrucomicrobiota (12.17%), and Acidobacteriota (7.87%). The diversity analysis metric showed that Heterodermia contained the highest bacterial species richness. Within the lichens, Ramalina conduplicans and Cladonia rappii showed a distinct bacterial community from the other lichen species. The community of lichen-associated actinobacteria was investigated as a potential source of synthesized biologically active compounds. From the total Operational Taxonomic Units (OTUs) found across the ten different lichen samples, 13.21% were identified as actinobacteria, including the rare actinobacterial genera that are not commonly found, such as Pseudonocardia, Kineosporia, Dactylosporangium, Amycolatopsis, Actinoplanes, and Streptosporangium. Evaluation of the pretreatment method (heat, air-drying, phenol, and flooding) and isolation media used for the culture-dependent actinobacterial isolation revealed that the different pretreatments combined with different isolation media were effective in obtaining several species of actinobacteria. However, metagenomics analyses revealed that there were still several strains, including rare actinobacterial species, that were not isolated. This research strongly suggests that lichens appear to be a promising source for obtaining actinobacteria.
The term phycobiome was recently introduced to designate all the microalgae (primary or non-primary) associated with
lichen symbioses. Abundant non-primary symbiotic microalgae are usually obtained from lichen isolations, confirming that
thalli are a source of biodiversity and new species. In this study, microalgae were isolated from thalli of Buellia zoharyi,
Ramalina farinacea and Parmotrema pseudotinctorum collected in the Iberian Peninsula and the Canary Islands. Excluding
Trebouxia phycobionts, 17 strains similar to Stichococcus (Prasiola clade) were obtained. Molecular identification was
carried out by nuclear ITS sequencing, and a phylogenetic tree was generated from these sequences, and grouping them
into 4 clades: Diplosphaera chodatti, Diplosphaera sp.1. Deuterostichocuccus sp.1. and Tritostichococcus coniocybes. It is
also noteworthy that Diplosphaera sp.1 was detected and isolated from three phylogenetically distant lichenized fungi (B.
zoharyi, R. farinacea and P. pseudotinctorum), which were sampled in ecologically different localities, namely Tenerife,
La Gomera and Castellón. These results reinforce the idea of the constant presence of certain microalgae associated with
the lichen thalli which, despite not being the main primary photobiont, probably form part of the lichen’s phycobiomes.
Lichens are mutually symbiotic systems consisting of fungal and algal symbionts. While diverse lichen-forming fungal species are known, limited species of algae form lichens. Plasticity in the combination of fungal and algal species with different eco-physiological properties may contribute to the worldwide distribution of lichens, even in extreme habitats. Lichens have been studied systematically for more than 200 years; however, plasticity in fungal–algal/cyanobacterial symbiotic combinations is still unclear. In addition, the association between non-cyanobacterial bacteria and lichens has attracted attention in recent years. The types, diversity, and functions of lichen-associated bacteria have been studied using both culture-based and culture-independent methods. This review summarizes the history of systematic research on lichens and lichen-associated bacteria and provides insights into the current status of research in this field.
