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Diverse hypolithic refuge communities in the McMurdo Dry Valleys

Published online by Cambridge University Press:  02 December 2010

Don A. Cowan*
Affiliation:
Institute for Microbial Biotechnology and Metagenomics, University of the Western Cape, Bellville 7535, Cape Town, South Africa
Nuraan Khan
Affiliation:
Institute for Microbial Biotechnology and Metagenomics, University of the Western Cape, Bellville 7535, Cape Town, South Africa
Stephen B. Pointing
Affiliation:
School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, China
S. Craig Cary
Affiliation:
Department of Biological Sciences, University of Waikato, Hamilton, New Zealand

Abstract

Hyper-arid deserts present extreme challenges to life. The environmental buffering provided by quartz and other translucent rocks allows hypolithic microbial communities to develop on sub-soil surfaces of such rocks. These refuge communities have been reported, for many locations worldwide, to be predominantly cyanobacterial in nature. Here we report the discovery in Antarctica’s hyper-arid McMurdo Dry Valleys of three clearly distinguishable types of hypolithic community. Based on gross colonization morphology and identification of dominant taxa, we have classified hypolithic communities as Type I (cyanobacterial dominated), Type II (fungal dominated) and Type III (moss dominated). This discovery supports a growing awareness of the high biocomplexity in Antarctic deserts, emphasizes the possible importance of cryptic microbial communities in nutrient cycling and provides evidence for possible successional community processes within a cold arid landscape.

Type
Research Article
Copyright
Copyright © Antarctic Science Ltd 2010

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References

Aislabie, J.M., Chhour, K.-L., Saul, D.J., Miyauchi, S., Ayton, J., Paetzold, R.F. Balks, M.R. 2006. Dominant bacteria in soils of Marble Point and Wright Valley, Victoria Land, Antarctica. Soil Biology & Biochemistry, 38, 30413056.CrossRefGoogle Scholar
Bardgett, R.D. Walker, L.R. 2004. Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biology & Biochemistry, 36, 555559.CrossRefGoogle Scholar
Bardgett, R.D., Bowman, W.D., Kaufmann, R. Schmidt, S.K. 2005. A temporal approach to linking aboveground and belowground ecology. Trends in Ecology & Evolution, 20, 634641.CrossRefGoogle ScholarPubMed
Bardgett, R.D., Richter, A., Bol, R., Garnett, M.H., Baumler, R., Xu, X., Lopez-Capel, E., Manning, D.A.C., Hobbs, P.J., Hartley, I.R. Wanek, W. 2007. Heterotrophic microbial communities use ancient carbon following glacial retreat. Biology Letters, 3, 487490.Google Scholar
Berner, T. Evenari, M. 1978. The influence of temperature and light penetration on the abundance of the hypolithic algae in the Negev Desert of Israel. Oecologia, 33, 255260.CrossRefGoogle ScholarPubMed
Bockheim, J.G. 1997. Properties and classification of cold desert soils from Antarctica. Soil Science Society of America Journal, 61, 224231.CrossRefGoogle Scholar
Boyd, W.L., Rothenberg, I. Boyd, J.W. 1970. Soil microorganisms at Paradise Harbor, Antarctica. Ecology, 51, 10401045.CrossRefGoogle Scholar
Broady, P.A. 1981. The ecology of sublithic terrestrial algae at the Vestfold Hills, Antarctica. British Phycological Journal, 16, 231240.CrossRefGoogle Scholar
Broady, P.A. 2005. The distribution of terrestrial and hydro-terrestrial algal association at three contrasting locations in southern Victoria Land, Antarctica. Algalogical Studies, 118, 95112.Google Scholar
Cameron, R., Morelli, F.A. Johnson, R.M. 1972. Bacterial species in soil and air of the Antarctic continent. Antarctic Journal of the United States, 7, 187189.Google Scholar
Cockell, C.S. Stokes, M.D. 2004. Widespread colonization by polar hypoliths. Nature, 431, 414.Google Scholar
Cockell, C.S., McKay, C.P., Warren-Rhodes, K. Horneck, G. 2008. Ultraviolet radiation-induced limitation to epilithic microbial growth in arid deserts: dosimetric experiments in the hyperarid core of the Atacama Desert. Journal of Photochemistry & Photobiology, B90, 7987.Google Scholar
Cordonnier, T., Courband, B. Franc, A. 2006. The effect of colonization and competition processes on the relation between disturbance and diversity in plant communities. Journal of Theoretical Biology, 243, 112.Google Scholar
Cowan, D.A. Ah Tow, L. 2004. Endangered Antarctic environments. Annual Reviews in Microbiology, 58, 649690.CrossRefGoogle ScholarPubMed
Cowan, D.A., Russell, N.J., Mamais, A. Sheppard, D.M. 2002. Antarctic dry valley mineral soils contain unexpectedly high levels of microbial biomass. Extremophiles, 6, 431436.CrossRefGoogle ScholarPubMed
Diez, B., Pedros-Alio, C., Marsh, T.L. Massana, R. 2001. Application of denaturing gradient gel electrophoresis (DGGE) to study the diversity of marine picoeukaryotic assemblages and comparison of DGGE with other molecular techniques. Applied & Environmental Microbiology, 67, 29422951.Google Scholar
Friedmann, E.I. Ocampo, R. 1976. Endolithic blue-green algae in the dry valleys: primary producers in the Antarctic desert ecosystem. Science, 193, 12471249.CrossRefGoogle ScholarPubMed
Halkka, O., Raatikainen, M. Halkka, L. 1974. The founder principle, founder selection, and evolutionary divergence and convergence in natural populations of Philaenus. Hereditas, 78, 7384.Google Scholar
Hansen, M.C., Tolker-Nielsen, T., Givskov, M. Molin, S. 1998. Biased 16S rDNA PCR amplification caused by interference from DNA flanking the template region. FEMS Microbiology Ecology, 26, 141149.CrossRefGoogle Scholar
Hopkins, D.W., Sparrow, A.D., Elberling, B., Gregorich, E.G., Novis, P.M., Greenfield, L.G. Tilston, E.L. 2006. Carbon, nitrogen and temperature controls on microbial activity in soils from an Antarctic dry valley. Soil Biology & Biochemistry, 38, 31303140.CrossRefGoogle Scholar
Hughes, K.A. Lawley, B. 2003. A novel Antarctic microbial endolithic community within gypsum crusts. Environmental Microbiology, 5, 555565.CrossRefGoogle ScholarPubMed
Khan, N. 2009. Characterisation of microbial communities associated with hypolithic environments in Antarctic dry valley soils. PhD thesis, University of the Western Cape, 216 pp. [Unpublished.].Google Scholar
Nienow, J.A. Friedmann, E.I. 1993. Terrestrial lithophytic (rock) communities. In Friedmann, E.I., ed. Antarctic microbiology. New York: Wiley-Liss, 343412.Google Scholar
Onofri, S., Selbmann, L., Zucconi, L. Pagano, S. 2004. Antarctic microfungi as models for exobiology. Planetary & Space Science, 52, 229237.CrossRefGoogle Scholar
Pointing, S.B., Warren-Rhodes, K.A., Lacap, D.C., Rhodes, K.L. McKay, C.P. 2007. Hypolithic community shifts occur as a result of liquid water availability along environmental gradients in China’s hot and cold hyperarid deserts. Environmental Microbiology, 9, 414424.CrossRefGoogle ScholarPubMed
Pointing, S.B., Chan, Y., Lacap, D.C., Lau, M.C.Y., Jirgens, J.A. Farrell, R.L. 2009. Highly specialized microbial diversity in hyper-arid polar desert. Proceedings of the National Academy of Science of the United States, 106, 19 96419 969.Google Scholar
Reysenbach, A.-L. Pace, N.R. 1995. Reliable amplification of hyperthermophilic archaeal 16S rRNA genes by the polymerase chain reaction. In Robb, F.T. & Place, A.R., eds. Archaea: a laboratory manual - thermophiles. Cold Spring Harbour, NY: Cold Spring Harbour Laboratory Press, 101107.Google Scholar
Schlesinger, W.H., Pippen, J.S., Wallenstein, M.D., Hofmockel, K.S., Klepeis, D.M. Mahall, B.E. 2003. Community composition and photosynthesis by photoautotrophs under quartz pebbles, southern Mojave Desert. Ecology, 84, 32223231.Google Scholar
Skotnicki, M.L., Ninham, J.A. Selkirk, P.M. 2000. Genetic diversity, mutagenesis and dispersal of Antarctic mosses - a review of progress with molecular studies. Antarctic Science, 12, 363373.Google Scholar
Smith, J.J., Ah Tow, L., Stafford, W., Cary, C. Cowan, D.A. 2006. Bacterial diversity in three different Antarctic cold desert mineral soils. Microbial Ecology, 51, 413421.Google Scholar
Smith, M.C., Bowman, J.P., Scott, F.J. Line, M.A. 2000. Sublithic bacteria associated with Antarctic quartz stones. Antarctic Science, 12, 177184.Google Scholar
Tscherko, D., Rustemeier, J., Richter, A., Wanek, W. Kandeler, E. 2003. Functional diversity of the soil microflora in primary succession across two glacier forelands. European Journal of Soil Science, 54, 685696.CrossRefGoogle Scholar
Vishniac, H.S. 1993. The microbiology of Antarctic soils. In Friedmann, E.I., ed. Antarctic microbiology. New York: Wiley-Liss, 343412.Google Scholar
Walker, L.R. del Moral, R. 2003. Primary succession and ecosystem rehabilitation. Cambridge: Cambridge University Press, 456 pp.Google Scholar
Warren-Rhodes, K.A., Rhodes, K.L., Pointing, S.B., Ewing, S.A., Lacap, D.C., Gomez-Silva, B., Amundson, R., Friedmann, E.I. McKay, C.P. 2006. Hypolithic cyanobacteria, dry limit of photosynthesis, and microbial ecology in the hyperarid Atacama Desert. Microbial Ecology, 52, 389398.CrossRefGoogle ScholarPubMed
Warren-Rhodes, K.A., Rhodes, K.L., Boyle, L.N., Pointing, S.B., Chen, Y., Liu, S., Zhuo, P. McKay, C.P. 2007. Cyanobacterial ecology across environmental gradients and spatial scales in China’s hot and cold deserts. FEMS Microbiology Ecology, 61, 470482.CrossRefGoogle ScholarPubMed
Wood, S.A., Rueckert, A., Cowan, D.A. Cary, S.C. 2008. Sources of edaphic cyanobacterial diversity in the dry valleys of eastern Antarctica. The ISME Journal, 2, 308320.Google Scholar
Wong, K.Y., Lau, M.C.Y., Lacap, D.C., Aitchison, J.C., Cowan, D.A. Pointing, S.B. 2010. Hypolithic colonization of quartz pavement in the high altitude tundra of central Tibet. Microbial Ecology, 10.1007/s00248010-9653-2.Google Scholar