Abstract
BackgroundCryptoendolithic 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.).ResultsA 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.ConclusionsOur 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.Ar7T6ZUsn22t2KkUgdSXvLVideo abstract
Highlights
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
Metagenomic assembly identifies novel bacterial species and broadly expands the tree of life Using shotgun sequencing, we produced more than 10 million contigs that were binned into a total of 1660 metagenome-assembled genomes (MAGs), among which 497 were identified as bacterial and none as archaeal
Species-level (95% ANI cutoff, see the “Methods” section) dereplication of the MAGs produced a set of 269 clusters—or candidate bacterial species (CBS)—each represented by the MAG of highest quality
Summary
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. Nextgeneration sequencing studies have brought new insights into their composition, showing that lichens in the Lecanoromycetes and free-living fungi in the Dothideomycetes (Ascomycota) are the dominant eukaryotes, while Actinobacteria and Proteobacteria are the most abundant prokaryotes [12, 13] Due to their ubiquity in deserts and low taxonomic complexity and biodiversity [14], endoliths are important study systems to understand evolutionary processes in the early history of life, to model how life evolves during the progression of desertification and when the extreme aridity approaches the limits of life, providing a model for searching life elsewhere in the solar system. The understanding of the microbial biodiversity in these communities is limited and our comprehension about their physiology, evolution, and stress responses is still at its infancy [15]
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