Abstract
The harsh environmental conditions of the ice-free regions of Continental Antarctica are considered one of the closest Martian analogues on Earth. There, rocks play a pivotal role as substratum for life and endolithism represents a primary habitat for microorganisms when external environmental conditions become incompatible with active life on rock surfaces, allowing life to spread throughout these regions with extreme temperatures and low water availability. Previous research concluded that altitude and distance from sea do not play as driving factors in shaping microbial abundance and diversity, while sun exposure was hypothesized as significant parameter influencing endolithic settlement and development. With this in mind, eight localities were visited in the Victoria Land along an altitudinal transect from 834 to 3100 m a.s.l. and 48 differently sun-exposed rocks were collected. We explored our hypothesis that changes in sun exposure translate to shifts in community composition and abundances of main biological compartments (fungi, algae and bacteria) using Denaturing Gel Gradient Electrophoresis and quantitative PCR techniques. Major changes in community composition and abundance occurred between north and south sun-exposed samples. As Antarctic endolithic ecosystems are extremely adapted and specialized but scarcely resilient to external perturbation, any shifts in community structure may serve as early-alarm systems of climate change; our findings will be of wide interest for microbial ecologists of extreme environments such as arid and hyper-arid area.
References
Bekryaev RV, Polyakov IV, Alexeev VA (2010) Role of polar amplification in long-term surface air temperature variations and modern Arctic warming. J Climate 23(14):3888–3906. https://doi.org/10.1175/2010JCLI3297.1
Bell RA (1993) Cryptoendolithic algae of hot semiarid lands and deserts. J Phycol 29:133–139. https://doi.org/10.1111/j.00223646.1993.00133.x
Bhatta KP, Grytnes JA, Vetaas OR (2018) Downhill shift of alpine plant assemblages under contemporary climate and land-use changes. Ecosphere 9(1):e02084. https://doi.org/10.1002/ecs2.2084
Cary SC, McDonald IR, Barrett JE, Cowan DA (2010) On the rocks: the microbiology of Antarctic dry valley soils. Nat Rev Microbiol 8:129–138. https://doi.org/10.1038/nrmicro2281
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Coleine C, Stajich JE, Zucconi L, Onofri S, Pombubpa N, Egidi E et al (2018a) Antarctic cryptoendolithic fungal communities are highly adapted and dominated by Lecanoromycetes and Dothideomycetes. Front Microbiol 9:1392. https://doi.org/10.3389/fmicb.2018.01392
Coleine C, Zucconi L, Onofri S, Pombubpa N, Stajich J, Selbmann L (2018b) Sun exposure shapes functional grouping of fungi cryptoendolithic Antarctic communities. Life 8(2):19. https://doi.org/10.3390/life8020019
Coleine C, Gevi F, Fanelli G, Onofri S, Timperio AM, Selbmann L (2019) Metabolic responses in opposite sun-exposed Antarctic cryptoendolithic communities. BioRxiv 725663: https://doi.org/10.1101/725663
Cowan D, Tow L (2004) Endangered Antarctic environments. Annu Rev Microbiol 58:649–690. https://doi.org/10.1146/annurev.micro.57.030502.090811
Cowan DA, Makhalanyane TP, Dennis PG, Hopkins DW (2014) Microbial ecology and biogeochemistry of continental Antarctic soils. Front Microbiol 5:154. https://doi.org/10.3389/fmicb.2014.00154
Deegenaars ML, Watson K (1998) Heat shock response in psychrophilic and psychrotrophic yeast from Antarctica. Extremophiles 2(1):41–50
Descamps S, Aars J, Fuglei E, Kovacs KM, Lydersen C, Pavlova O et al (2017) Climate change impacts on wildlife in a High Arctic Archipelago-Svalbard. Norway Global Change Biol 23(2):490–502. https://doi.org/10.1111/gcb.13381
De Vries FT, Liiri ME, Bjørnlund L, Bowker MA, Christensen S, Setälä HM, Bardgett RD (2012) Land use alters the resistance and resilience of soil food webs to drought. Nat Clim Change 2(4):276. https://doi.org/10.1038/nclimate1368
Egidi E, De Hoog GS, Isola D, Onofri S, Quaedvlieg W, Vries De et al (2014) Phylogeny and taxonomy of meristematic rock-inhabiting black fungi in the dothidemycetes based on multi-locus phylogenies. Fungal Divers 65:127–165. https://doi.org/10.1007/s13225-013-0277-y
Farrell RL, Arenz BE, Duncan SM, Held BW, Jurgens JA, Blanchette RA (2011) Introduced and indigenous fungi of the Ross Island historic huts and pristine areas of Antarctica. Polar Biol 34:1669–1677
Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71(7):4117–4120. https://doi.org/10.1128/AEM.71.7.4117-4120.2005
Friedmann EI, Ocampo R (1976) Endolithic blue-green algae in dry valleys-primary producers in Antarctic desert ecosystem. Science 193:1247–1249. https://doi.org/10.1126/science.193.4259.1247
Friedmann EI (1977) Microorganisms in Antarctic desert rocks from dry valleys and Dufek Massif. Antarctic J US 12(4):26–29
Friedmann EI (1982) Endolithic microorganisms in the Antarctic cold desert. Science 215:1045–1053
Friedmann EI, Weed R (1987) Microbial trace-fossil formation, biogenous, and abiotic weathering in the Antarctic cold desert. Science 236(4802):703–705. https://doi.org/10.1126/science.215.4536.1045
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2(2):113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Gordon H, Haygarth PM, Bardgett RD (2008) Drying and rewetting effects on soil microbial community composition and nutrient leaching. Soil Biol Biochem 40(2):302–311. https://doi.org/10.1016/j.soilbio.2007.08.008
Helms G, Friedl T, Rambold G, Mayrhofer H (2001) Identification of photobionts from the lichen family Physciaceae using algal-specific ITS rDNA sequencing. Lichenologist 33:73–86. https://doi.org/10.1006/lich.2000.0298
Horowitz NH, Cameron RE, Hubbard JS (1972) Microbiology of the dry valleys of Antarctica. Science 176(4032):242–245. https://doi.org/10.1126/science.176.4032.242
Kovalski-Mitter E, de Freitas R, Germida JJ (2018) Microbial communities associated with barley growing in an oil sands reclamation area in Alberta. Canada Can J Microbiol 64(12):1004–1019. https://doi.org/10.1139/cjm-2018-0324
Magan N (2007) Fungi in extreme environments The Mycota 4:85–103. https://doi.org/10.1016/j.funeco.2012.04.003
McKay CP, Friedmann EI (1985) The cryptoendolithic microbial environment in the Antarctic cold desert: temperature variations in nature. Polar Biol 4(1):19–25. https://doi.org/10.1007/BF00286813
Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
NAS (2011) Future science opportunities in Antarctica and the Southern Ocean (report in brief). National Academy of Sciences https://wwwdels.nas.edu/prb.
Nienow JA, Friedmann EI (1993) Terrestrial lithophytic (rock) communities. In: Friedmann EI (ed) Antarctic microbiology. Wiley-Liss, New York, pp 343–412
Olech M, Chwedorzewska KJ (2011) Short note: the first appearance and establishment of an alien vascular plant in natural habitats on the forefield of a retreating glacier in Antarctica. Antarct Sci 23:153–154. https://doi.org/10.1017/S0954102010000982
Onofri S, Barreca D, Selbmann L, Isola D, Rabbow E, Horneck G et al (2008) Resistance of Antarctic black fungi and cryptoendolithic communities to simulated space and Mars conditions. Stud Mycol 61:99–109. https://doi.org/10.3114/sim.2008.61.10
Onofri S, de la Torre R, de Vera JP, Ott S, Zucconi L, Selbmann L (2012) Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12:508–516. https://doi.org/10.1089/ast.2011.0736
Onofri S, de Vera JP, Zucconi L, Selbmann L, Scalzi G, Venkateswaran KJ et al (2015) Survival of Antarctic cryptoendolithic fungi in simulated martian conditions nn board the international space station. Astrobiology 15:1052–1059. https://doi.org/10.1089/ast.2015.1324
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Piercey-Normore MD, De Priest PT (2001) Algal switching among lichen symbioses. Am J Bot 88(8):1490–1498. https://doi.org/10.2307/3558457
Quintal H, Head J, Palumbo A, Dickson J (2018) McMurdo dry valleys: exploring Antarctica as a Mars analogue: in lunar and planetary science conference, 49.
Raeymaekers L (2000) Basic principles of quantitative PCR. Molecular Biotechnol 15(2):115–122. https://doi.org/10.1385/MB:15:2:115
Selbmann L, de Hoog GS, Mazzaglia A, Friedmann EI, Onofri S et al (2005) Fungi at the edge of life: cryptoendolithic black fungi from Antarctic deserts. Stud Mycol 51:1–32
Selbmann L, de Hoog GS, Zucconi L, Isola D, Ruisi S, van den Ende AG et al (2008) Drought meets acid: three new genera in a dothidealean clade of extremotolerant fungi. Stud Mycol 61:1–20. https://doi.org/10.3114/sim.2008.61.01
Selbmann L, Isola D, Fenice M, Zucconi L, Sterflinger K, Onofri S (2012) Potential extinction of Antarctic endemic fungal species as a consequence of Global Warming. Science Total Environ 438:127–134. https://doi.org/10.1016/j.scitotenv.2012.08.027
Selbmann L, Egidi E, Isola D, Onofri S, Zucconi L, de Hoog GS et al (2013) Biodiversity, evolution and adaptation of fungi in extreme environments. Plant Biosyst 147(1):237–246. https://doi.org/10.1080/11263504.2012.753134
Selbmann L, Onofri S, Coleine C, Buzzini P, Canini F, Zucconi L (2017) Effect of environmental parameters on biodiversity of the fungal component in the lithic Antarctic communities. Extremophiles 21:1069–1080. https://doi.org/10.1007/s00792-017-0967-6
Selbmann L, Pacelli C, Zucconi L, Dadachova E, Moeller R, de Vera JP, Onofri S (2018) Resistance of an Antarctic cryptoendolithic black fungus to radiation gives new insights of astrobiological relevance. Fungal Biol 122(6):546–554. https://doi.org/10.1016/j.funbio.2017.10.012
Steig EJ, Schneider DP, Rutherford SD, Mann ME, Comiso JC, Shindell DT (2009) Warming of the Antarctic ice-sheet surface since the 1957 International Geophysical Year. Nature 457(7228):459. https://doi.org/10.1038/nature07669
Turner J, Colwell SR, Marshall GJ, Lachlan-Cope TA, Carleton AM, Jones PD et al (2005) Antarctic climate change during the last 50 years. Int J Climatol 25:279–294. https://doi.org/10.1002/joc.1130
Turner J, Overland JE, Walsh JE (2007) An Arctic and Antarctic perspective on recent climate change. Int J Climatol 27:277–293. https://doi.org/10.1002/joc.1406
Valášková V, Baldrian P (2009) Denaturing gradient gel electrophoresis as a fingerprinting method for the analysis of soil microbial communities. Plant Soil Environ 55(10):413–423. https://doi.org/10.17221/132/2009-PSE
Venkateswaran A, McFarlan SC, Ghosal D, Minton KW, Vasilenko A, Makarova K et al (2000) Physiologic determinants of radiation resistance inDeinococcus radiodurans. Applied Environ Microbiol 66(6):2620–2626
Walker JJ, Spear JR, Pace NR (2005) Geobiology of a microbial endolithic community in the Yellowstone geothermal environment. Nature 434:1011–1014. https://doi.org/10.1038/nature03447
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, New York, pp 315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Yao T, Thompson LG, Mosbrugger V, Zhang F, Ma Y, Luo T et al (2012) Third pole environment (TPE). Environ Dev 3:52–64. https://doi.org/10.1016/j.envdev.2012.04.002
Yang K, Wu H, Qin J, Lin C, Tang W, Chen Y (2014) Recent climate changes over the Tibetan Plateau and their impacts on energy and water cycle: A review. Glob Planet Change 112:79–91. https://doi.org/10.1016/j.gloplacha.2013.12.001
Zheng J, Liang R, Zhang L, Wu C, Zhou R, Liao X (2013) Characterization of microbial communities in strong aromatic liquor fermentation pit muds of different ages assessed by combined DGGE and PLFA analyses. Food Res Int 54(1):660–666. https://doi.org/10.1016/j.foodres.2013.07.058
Zucconi L, Onofri S, Cecchini C, Isola D, Ripa C, Fenice M et al (2016) Mapping the lithic colonization at the boundaries of life in Northern Victoria Land. Antarctica Polar Biol 39(1):91–102. https://doi.org/10.1007/s00300-014-1624-5
Acknowledgements
L.S., C.C. and L.Z. wish to thank the Italian National Program for Antarctic Researches (PNRA) for funding sampling campaigns and researches activities in Italy in the frame of PNRA Projects. The Italian Antarctic National Museum (MNA) is acknowledged for financial support to the Mycological Section on the MNA for preserving Antarctic rock samples analysed in this study and stored in the Culture Collection of Fungi from Extreme Environments (CCFEE), University of Tuscia, Italy.
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Supplementary file2 (TIF 5472 kb)—Dendrogram obtained by Unweighted Pair Group Method using Arithmetic average (UPGMA) based on the DGGE profiles of the bacterial component of the endolithic communities.
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Coleine, C., Stajich, J.E., Zucconi, L. et al. Sun exposure drives Antarctic cryptoendolithic community structure and composition. Polar Biol 43, 607–615 (2020). https://doi.org/10.1007/s00300-020-02650-1
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DOI: https://doi.org/10.1007/s00300-020-02650-1