Peculiar genomic traits in the stress-adapted cryptoendolithic Antarctic fungus Friedmanniomyces endolithicus

Coleine, Claudia; Masonjones, Sawyer; Sterflinger, Katja; Onofri, Silvano; Selbmann, Laura; Stajich, Jason E.

doi:10.1016/j.funbio.2020.01.005

Cited by 26 publications

(24 citation statements)

References 83 publications

(76 reference statements)

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“…Despite the arguably lower sensitivity of shotgun metagenomics compared with amplicon-based methods for biodiversity description [48,79], our study confirms earlier findings of high site variability between prokaryotic communities in Antarctica soils [80]. The presence of recurrent species in the Antarctic cryptoendolithic communities has been also observed for the fungal counterpart: for instance, the endemic black fungus Friedmanniomyces endolithicus has been reported in almost all samples collected in the Victoria Land in more than 20 years of Antarctic Campaigns [81,82], indicating a high degree of adaptation to the prohibitive environmental conditions of this area.…”

Section: Discussionsupporting

confidence: 87%

Pre-Cambrian roots of novel Antarctic cryptoendolithic bacterial lineages

et al. 2021

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Background Cryptoendolithic communities are microbial ecosystems dwelling inside porous rocks that are able to persist at the edge of the biological potential for life in the ice-free areas of the Antarctic desert. These regions include the McMurdo Dry Valleys, often accounted as the closest terrestrial counterpart of the Martian environment and thought to be devoid of life until the discovery of these cryptic life-forms. Despite their interest as a model for the early colonization by living organisms of terrestrial ecosystems and for adaptation to extreme conditions of stress, little is known about the evolution, diversity, and genetic makeup of bacterial species that reside in these environments. Using the Illumina Novaseq platform, we generated the first metagenomes from rocks collected in Continental Antarctica over a distance of about 350 km along an altitudinal transect from 834 up to 3100 m above sea level (a.s.l.). Results A total of 497 draft bacterial genome sequences were assembled and clustered into 269 candidate species that lack a representative genome in public databases. Actinobacteria represent the most abundant phylum, followed by Chloroflexi and Proteobacteria. The “Candidatus Jiangella antarctica” has been recorded across all samples, suggesting a high adaptation and specialization of this species to the harshest Antarctic desert environment. The majority of these new species belong to monophyletic bacterial clades that diverged from related taxa in a range from 1.2 billion to 410 Ma and are functionally distinct from known related taxa. Conclusions Our findings significantly increase the repertoire of genomic data for several taxa and, to date, represent the first example of bacterial genomes recovered from endolithic communities. Their ancient origin seems to not be related to the geological history of the continent, rather they may represent evolutionary remnants of pristine clades that evolved across the Tonian glaciation. These unique genomic resources will underpin future studies on the structure, evolution, and function of these ecosystems at the edge of life.

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Section: Discussionsupporting

confidence: 87%

Pre-Cambrian roots of novel Antarctic cryptoendolithic bacterial lineages

et al. 2021

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“…To date, the halophilic black fungus Hortaea werneckii remains the only described example of a recent genome duplication or change in ploidy (Lenassi et al 2013;Sinha et al 2017;Gostinčar et al 2018). Evidence of genomic changes that help organisms cope with low temperature, salt, X-rays, and DNA damage was found in F. endolithicus and confirms that this genus has exceptional polyextreme tolerance and the capacity to survive across a wide variety of stresses (Coleine et al 2020c). One fungus, F. endolithicus, is the most widespread and abundant species in Antarctic cryptoendolithic communities, suggesting a high degree of adaptation to the prohibitive environmental conditions of the Antarctic desert.…”

Section: Rock Black Fungi Represent the Excellence In The Hyperarid Amentioning

confidence: 84%

“…The genomes of Rachicladosporium antarcticum CCFEE 5527, Rachicladosporium sp. CCFEE 5018, Exophiala mesophila CCFEE 6314, Horteaea thailandica CCFEE 6315, C. antarcticus CCFEE 534, C. minteri CCFEE 5187, F. endolithicus CCFEE 5311, and F. simplex CCFEE 5184 have been published recently Coleine et al 2017Coleine et al , 2019Coleine et al , 2020c. Most of these fungi have a higher DNA G+C content than other black fungi (Teixeira et al 2017), and the genomes (35-50 Mbp) and proteomes (15 000-20 000 predicted protein-coding genes) are generally quite large.…”

Section: Rock Black Fungi Represent the Excellence In The Hyperarid Amentioning

confidence: 99%

Beyond the extremes: Rocks as ultimate refuge for fungi in drylands

et al. 2020

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In an era of rapid climate change and expansion of desertification, the extremely harsh conditions of drylands are a true challenge for microbial life. Under drought conditions, where most life forms cannot survive, rocks represent the main refuge for life. Indeed, the endolithic habitat provides thermal buffering, physical stability, and protection against incident ultraviolet (UV) radiation and solar radiation and, to some extent, ensures water retention to microorganisms. The study of these highly specialized extreme-tolerant and extremophiles may provide tools for understanding microbial interactions and processes that allow them to keep their metabolic machinery active under conditions of dryness and oligotrophy that are typically incompatible with active life, up to the dry limits for life. Despite lithobiontic communities being studied all over the world, a comprehensive understanding of their ecology, evolution, and adaptation is still nascent. Herein, we survey the fungal component of these microbial ecosystems. We first provide an overview of the main defined groups (i.e., lichen-forming fungi, black fungi, and yeasts) of the most known and studied Antarctic endolithic communities that are almost the only life forms ensuring ecosystem functionality in the ice-free areas of the continent. For each group, we discuss their main traits and their diversity. Then, we focus on the fungal taxonomy and ecology of other worldwide endolithic communities. Finally, we highlight the utmost importance of a global rock survey in order to have a comprehensive view of the diversity, distribution, and functionality of these fungi in drylands, to obtain tools in desert area management, and as early alarm systems to climate change.

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“…Proteomic studies have highlighted that responses to sub-optimal temperature are related to a downregulation of response rather than a heat-shock protein over-expression [58] and the ability of this fungus to tolerate acute doses of gamma radiation (up to 400 Gy) was also demonstrated [59]. Recently, the whole genome Friedmanniomyces endolithicus CCFEE 5311 was sequenced and assembled, resulting in 46.75 Mbp and 18,027 predicted proteins; genomic traits in response to salt, X-rays, cold and DNA damage stresses have been identified, confirming exceptional poly-heterotolerance of this species to survive across a wide variety of stresses [60].…”

Section: Discussionmentioning

confidence: 81%

Endolithic Fungal Species Markers for Harshest Conditions in the McMurdo Dry Valleys, Antarctica

Coleine

Pombubpa

Zucconi

et al. 2020

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The microbial communities that inhabit lithic niches inside sandstone in the Antarctic McMurdo Dry Valleys of life’s limits on Earth. The cryptoendolithic communities survive in these ice-free areas that have the lowest temperatures on Earth coupled with strong thermal fluctuations, extreme aridity, oligotrophy and high levels of solar and UV radiation. In this study, based on DNA metabarcoding, targeting the fungal Internal Transcribed Spacer region 1 (ITS1) and multivariate statistical analyses, we supply the first comprehensive overview onto the fungal diversity and composition of these communities sampled over a broad geographic area of the Antarctic hyper-arid cold desert. Six locations with surfaces that experience variable sun exposure were sampled to compare communities from a common area across a gradient of environmental pressure. The Operational Taxonomic Units (OTUs) identified were primarily members of the Ascomycota phylum, comprised mostly of the Lecanoromycetes and Dothideomycetes classes. The fungal species Friedmanniomyces endolithicus, endemic to Antarctica, was found to be a marker species to the harshest conditions occurring in the shady, south exposed rock surfaces. Analysis of community composition showed that sun exposure was an environmental property that explained community diversity and structured endolithic colonization.

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Peculiar genomic traits in the stress-adapted cryptoendolithic Antarctic fungus Friedmanniomyces endolithicus

Cited by 26 publications

References 83 publications

Pre-Cambrian roots of novel Antarctic cryptoendolithic bacterial lineages

Pre-Cambrian roots of novel Antarctic cryptoendolithic bacterial lineages

Beyond the extremes: Rocks as ultimate refuge for fungi in drylands

Endolithic Fungal Species Markers for Harshest Conditions in the McMurdo Dry Valleys, Antarctica

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