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

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.

[1]  L. Selbmann,et al.  Specific adaptations are selected in opposite sun exposed Antarctic cryptoendolithic communities as revealed by untargeted metabolomics , 2020, PloS one.

[2]  J. Stajich,et al.  Peculiar genomic traits in the stress-adapted cryptoendolithic Antarctic fungus Friedmanniomyces endolithicus. , 2020, Fungal biology.

[3]  C. Rosa,et al.  Diversity, Distribution, and Ecology of Fungi in the Seasonal Snow of Antarctica , 2019, Microorganisms.

[4]  L. Selbmann,et al.  Metabolic responses in opposite sun-exposed Antarctic cryptoendolithic communities , 2019, bioRxiv.

[5]  J. Stajich,et al.  Sun exposure drives Antarctic cryptoendolithic community structure and composition , 2019, bioRxiv.

[6]  E. Rabbow,et al.  Survival, DNA, and Ultrastructural Integrity of a Cryptoendolithic Antarctic Fungus in Mars and Lunar Rock Analogs Exposed Outside the International Space Station. , 2019, Astrobiology.

[7]  I. Shuryak,et al.  Survival and redox activity of Friedmanniomyces endolithicus, an Antarctic endemic black meristematic fungus, after gamma rays exposure. , 2018, Fungal biology.

[8]  L. Selbmann,et al.  Roof-Inhabiting Cousins of Rock-Inhabiting Fungi: Novel Melanized Microcolonial Fungal Species from Photocatalytically Reactive Subaerial Surfaces , 2018, Life.

[9]  J. Stajich,et al.  Antarctic Cryptoendolithic Fungal Communities Are Highly Adapted and Dominated by Lecanoromycetes and Dothideomycetes , 2018, Front. Microbiol..

[10]  J. Stajich,et al.  Sun Exposure Shapes Functional Grouping of Fungi in Cryptoendolithic Antarctic Communities , 2018, Life.

[11]  E. Dadachova,et al.  Resistance of an Antarctic cryptoendolithic black fungus to radiation gives new insights of astrobiological relevance. , 2018, Fungal biology.

[12]  Jonathan M Palmer,et al.  Non-biological synthetic spike-in controls and the AMPtk software pipeline improve mycobiome data , 2018, PeerJ.

[13]  L. Selbmann,et al.  Effect of environmental parameters on biodiversity of the fungal component in lithic Antarctic communities , 2017, Extremophiles.

[14]  S. Cary,et al.  Endolithic microbial diversity in sandstone and granite from the McMurdo Dry Valleys, Antarctica , 2017, Polar Biology.

[15]  J. Welker,et al.  Changes in composition and abundance of functional groups of arctic fungi in response to long-term summer warming , 2016, Biology Letters.

[16]  S. Cary,et al.  Endolithic microbial diversity in sandstone and granite from the McMurdo Dry Valleys, Antarctica , 2016, Polar Biology.

[17]  Elke Rabbow,et al.  Survival of Antarctic Cryptoendolithic Fungi in Simulated Martian Conditions On Board the International Space Station. , 2015, Astrobiology.

[18]  Robert C. Edgar,et al.  Error filtering, pair assembly and error correction for next-generation sequencing reads , 2015, Bioinform..

[19]  L. Selbmann,et al.  Distributional records of Antarctic fungi based on strains preserved in the Culture Collection of Fungi from Extreme Environments CCFEE Mycological Section associated with the Italian National Antarctic Museum MNA. , 2015 .

[20]  C. Gueidan,et al.  Mountain tips as reservoirs for new rock-fungal entities: Saxomyces gen. nov. and four new species from the Alps , 2014, Fungal Diversity.

[21]  Kabir G. Peay,et al.  Sequence Depth, Not PCR Replication, Improves Ecological Inference from Next Generation DNA Sequencing , 2014, PloS one.

[22]  G. S. Hoog,et al.  Phylogeny and taxonomy of meristematic rock-inhabiting black fungi in the Dothideomycetes based on multi-locus phylogenies , 2014, Fungal Diversity.

[23]  Kessy Abarenkov,et al.  Fungal community analysis by high-throughput sequencing of amplified markers – a user's guide , 2013, The New phytologist.

[24]  Petr Baldrian,et al.  Estimation of fungal biomass in forest litter and soil , 2013 .

[25]  L. Selbmann,et al.  Biodiversity, evolution and adaptation of fungi in extreme environments , 2013 .

[26]  K. Sterflinger,et al.  Fungi in hot and cold deserts with particular reference to microcolonial fungi , 2012 .

[27]  L. Selbmann,et al.  Alteration of protein patterns in black rock inhabiting fungi as a response to different temperatures , 2012, Fungal biology.

[28]  Elke Rabbow,et al.  Survival of rock-colonizing organisms after 1.5 years in outer space. , 2012, Astrobiology.

[29]  L. Selbmann,et al.  Resistance to UV-B induced DNA damage in extreme-tolerant cryptoendolithic Antarctic fungi: detection by PCR assays. , 2011, Fungal biology.

[30]  I. Hogg,et al.  Global change and Antarctic terrestrial biodiversity , 2011, Polar Biology.

[31]  Josefino C. Comiso,et al.  Warming of the Antarctic ice-sheet surface since the 1957 International Geophysical Year , 2009, Nature.

[32]  A. Casadevall,et al.  Ionizing radiation: how fungi cope, adapt, and exploit with the help of melanin. , 2008, Current opinion in microbiology.

[33]  T. Green,et al.  Slowest to fastest: Extreme range in lichen growth rates supports their use as an indicator of climate change in Antarctica , 2007 .

[34]  Diana H. Wall,et al.  Diversity and distribution of Victoria Land biota , 2006 .

[35]  Norman R. Pace,et al.  Microbial Diversity of Cryptoendolithic Communities from the McMurdo Dry Valleys, Antarctica , 2003, Applied and Environmental Microbiology.

[36]  Christopher P. McKay,et al.  Valley floor climate observations from the McMurdo dry valleys, Antarctica, 1986–2000 , 2002 .

[37]  C. Ascaso,et al.  Life, decay and fossilisation of endolithic microorganisms from the Ross Desert, Antarctica , 2001, Polar Biology.

[38]  L. Kappen Some aspects of the great success of lichens in Antarctica , 2000, Antarctic Science.

[39]  N. Gunde-Cimerman,et al.  Hypersaline waters in salterns - natural ecological niches for halophilic black yeasts. , 2000 .

[40]  H. Edwards,et al.  Proximal Analysis of Regolith Habitats and Protective Biomolecules in Situ by Laser Raman Spectroscopy: Overview of Terrestrial Antarctic Habitats and Mars Analogs , 2000 .

[41]  E. Friedmann,et al.  Endolithic Microorganisms in the Antarctic Cold Desert , 1982, Science.

[42]  E. Friedmann,et al.  Endolithic Blue-Green Algae in the Dry Valleys: Primary Producers in the Antarctic Desert Ecosystem , 1976, Science.

[43]  R. E. Cameron,et al.  Microbiology of the dry valleys of antarctica. , 1972, Science.

[44]  C. Schaefer,et al.  Rock-Inhabiting Fungi in Antarctica: New Frontiers of the Edge of Life , 2019, Fungi of Antarctica.

[45]  J. Handelsman,et al.  Beyond the Venn diagram: the hunt for a core microbiome. , 2012, Environmental microbiology.

[46]  Robert C. Edgar,et al.  Search and clustering orders of magnitude faster than BLAST , 2010 .

[47]  A. Gorbushina,et al.  Cellular responses of microcolonial rock fungi to long-term desiccation and subsequent rehydration , 2008, Studies in mycology.

[48]  G. Horneck,et al.  Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Martian conditions , 2008, Studies in mycology.

[49]  L. Selbmann,et al.  UvA-DARE (Digital Academic Repository) Drought meets acid: Three new genera in a dothidealean clade of extremotolerant , 2008 .

[50]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[51]  L. Selbmann,et al.  Fungi at the edge of life: cryptendolithic black fungi from Antarctic desert , 2005 .

[52]  G. S. Hoog,et al.  Fungi of the Antarctic: Evolution under extreme conditions , 2005 .

[53]  L. Selbmann,et al.  Antarctic microfungi as models for exobiology , 2004 .

[54]  J. Frisvad,et al.  Extremophilic fungi in arctic ice: a relationship between adaptation to low temperature and water activity , 2003 .

[55]  Ø. Hammer PAST - PAlaeontological STatistics , 2001 .

[56]  L. Kappen Plant Activity under Snow and Ice, with Particular Reference to Lichens , 1993 .

[57]  E. Friedmann,et al.  Life on Mars: how it disappeared (if it was ever there). , 1989, Advances in space research : the official journal of the Committee on Space Research.

[58]  E. H. Simpson Measurement of Diversity , 1949, Nature.