Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T04:19:34.226Z Has data issue: false hasContentIssue false

Insights into the metabolism of the high temperature microbial community of Tramway Ridge, Mount Erebus, Antarctica

Published online by Cambridge University Press:  17 February 2016

Chelsea J. Vickers
Affiliation:
International Centre for Terrestrial Antarctic Research, School of Science, Faculty of Science and Engineering, University of Waikato, Private Bag 3105, Hamilton, New Zealand
Craig W. Herbold
Affiliation:
International Centre for Terrestrial Antarctic Research, School of Science, Faculty of Science and Engineering, University of Waikato, Private Bag 3105, Hamilton, New Zealand
S. Craig Cary
Affiliation:
International Centre for Terrestrial Antarctic Research, School of Science, Faculty of Science and Engineering, University of Waikato, Private Bag 3105, Hamilton, New Zealand
Ian R. Mcdonald*
Affiliation:
International Centre for Terrestrial Antarctic Research, School of Science, Faculty of Science and Engineering, University of Waikato, Private Bag 3105, Hamilton, New Zealand
*
**corresponding author: [email protected]

Abstract

Mount Erebus is the most active volcano on the Antarctic continent, and it has the most geographically and physically isolated geothermal soil on Earth. Preliminary genetic analysis of the microbial community present in the 65°C subsurface soil of Tramway Ridge, on Mount Erebus, revealed a unique high temperature ecosystem, with the dominant members possessing little genetic similarity to known bacteria. This study investigated the metabolism and physiology of this intriguing ecosystem using physical-chemical soil surveying, community-based phenotypic arrays, nutritional enrichment experiments and pyrosequencing. Results have provided new insights into the metabolic requirements and putative roles of specific organisms, as well as the significance of specific carbon and nitrogen sources. In enrichment experiments bicarbonate slowed down an otherwise dramatic shift in community structure. This suggests that bicarbonate maintains the native community in vitro by supplying an essential inorganic compound that is utilized for slow, autotrophic growth. This approach shows potential as a model for future investigations of cultivation resistant thermophilic communities.

Type
Biological Sciences
Copyright
© Antarctic Science Ltd 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdo, Z., Schüette, U.M.E., Bent, S.J., Williams, C.J., Forney, L.J. & Joyce, P. 2006. Statistical methods for characterizing diversity of microbial communities by analysis of terminal restriction fragment length polymorphisms of 16S rRNA genes. Environmental Microbiology, 8, 929938.Google Scholar
Barker, P.F. & Burrell, J. 1977. Opening of Drake Passage. Marine Geology, 25, 1534.CrossRefGoogle Scholar
Barrett, J.E., Virginia, R.A., Wall, D.H., Cary, S.C., Adams, B.J., Hacker, A.L. & Aislabie, J.M. 2006. Co-variation in soil biodiversity and biogeochemistry in northern and southern Victoria Land, Antarctica. Antarctic Science, 18, 535548.Google Scholar
Blank, C.E., Cady, S.L. & Pace, N.R. 2002. Microbial composition of near-boiling silica-depositing thermal springs throughout Yellowstone National Park. Applied and Environmental Microbiology, 68, 51235135.Google Scholar
Broady, P.A. 1984. Taxonomic and ecological investigations of algae on steam-warmed soil on Mt Erebus, Ross Island, Antarctica. Phycologia, 23, 257271.Google Scholar
Calkins, J., Oppenheimer, C. & Kyle, P.R. 2008. Ground-based thermal imaging of lava lakes at Erebus volcano, Antarctica. Journal of Volcanology and Geothermal Research, 177, 695704.CrossRefGoogle Scholar
Costa, K.C., Navarro, J.B., Shock, E.L., Zhang, C.L.L., Soukup, D. & Hedlund, B.P. 2009. Microbiology and geochemistry of great boiling and mud hot springs in the United States Great Basin. Extremophiles, 13, 447459.Google Scholar
Dunbar, J., Takala, S., Barns, S.M., Davis, J.A. & Kuske, C.R. 1999. Levels of bacterial community diversity in four arid soils compared by cultivation and 16S rRNA gene cloning. Applied and Environmental Microbiology, 65, 16621669.CrossRefGoogle ScholarPubMed
Engel, A.S., Johnson, L.R. & Porter, M.L. 2013. Arsenite oxidase gene diversity among Chloroflexi and Proteobacteria from El Tatio Geyser Field, Chile. FEMS Microbiology Ecology, 83, 745756.Google Scholar
Georgacakis, D., Sievers, D.M. & Iannotti, E.L. 1982. Buffer stability in manure digesters. Agricultural Wastes, 4, 427441.CrossRefGoogle Scholar
Hansom, J.D. & Gordon, J.E. 1998. Antarctic environments and resources: a geographical perspective. Harlow: Addison Wesley Longman, 416 pp.Google Scholar
Hatzenpichler, R., Lebedeva, E.V., Spieck, E., Stoecker, K., Richter, A., Daims, H. & Wagner, M. 2008. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proceedings of the National Academy of Science of the United States of America, 105, 21342139.Google Scholar
Herbold, C.W., Lee, C.K., McDonald, I.R. & Cary, S.C. 2014. Evidence of global-scale aeolian dispersal and endemism in isolated geothermal microbial communities of Antarctica. Nature Communications, 5, 10.1038/ncomms4875.Google Scholar
Hudson, J.A. & Daniel, R.M. 1988. Enumeration of thermophilic heterotrophs in geothermally heated soils from Mount Erebus, Ross Island, Antarctica. Applied and Environmental Microbiology, 54, 622624.Google Scholar
Hudson, J.A., Daniel, R.M. & Morgan, H.W. 1989. Acidophilic and thermophilic Bacillus strains from geothermally heated Antarctic soil. FEMS Microbiology Letters, 60, 279282.Google Scholar
Hudson, J.A., Morgan, H.W. & Daniel, R.M. 1987. Numerical classification of some Thermus isolates from Icelandic hot springs. Systematic and Applied Microbiology, 9, 218223.Google Scholar
Lee, C.K., Barbier, B.A., Bottos, E.M., McDonald, I.R. & Cary, S.C. 2012. The Inter-Valley Soil Comparative Survey: the ecology of Dry Valley edaphic microbial communities. ISME Journal, 6, 10461057.CrossRefGoogle ScholarPubMed
Lesser, M.P., Barry, T.M. & Banaszak, A.T. 2002. Effects of UV radiation on a chlorophyte alga (Scenedesmus sp.) isolated from the fumarole fields of Mount Erebus, Antarctica. Journal of Phycology, 38, 473481.Google Scholar
Liao, P.-C., Huang, B.-H. & Huang, S. 2007. Microbial community composition of the Danshui river estuary of northern Taiwan and the practicality of the phylogenetic method in microbial barcoding. Microbial Ecology, 54, 497507.Google Scholar
McDonald, D., Price, M.N., Goodrich, J., Nawrocki, E.P., DeSantis, T.Z., Probst, A., Andersen, G.L., Knight, R. & Hugenholtz, P. 2012. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME Journal, 6, 610618.Google Scholar
Melick, D.R., Broady, P.A. & Rowan, K.S. 1991. Morphological and physiological characteristics of a nonheterocystous strain of the cyanobacterium Mastigocladus laminosus Cohn from fumarolic soil on Mt Erebus, Antarctica. Polar Biology, 11, 8189.Google Scholar
Meyer-Dombard, D.R., Swingley, W., Raymond, J., Havig, J., Shock, E.L. & Summons, R.E. 2011. Hydrothermal ecotones and streamer biofilm communities in the Lower Geyser Basin, Yellowstone National Park. Environmental Microbiology, 13, 22162231.Google Scholar
Parish, T.R. & Bromwich, D.H. 1991. Continental-scale simulation of the Antarctic katabatic wind regime. Journal of Climate, 4, 135146.Google Scholar
Quince, C., Lanzen, A., Davenport, R.J. & Turnbaugh, P.J. 2011. Removing noise from pyrosequenced amplicons. BMC Bioinformatics, 12, 10.1186/1471-2105-12-38.Google Scholar
Ramírez-Arcos, S., Fernández-Herrero, L.A., Marín, I. & Berenguer, J. 1998. Anaerobic growth, a property horizontally transferred by an Hfr-like mechanism among extreme thermophiles. Journal of Bacteriology, 180, 31373143.Google Scholar
Schloss, P.D., Westcott, S.L., Ryabin, T., Hall, J.R., Hartmann, M., Hollister, E.B., Lesniewski, R.A., Oakley, B.B., Parks, D.H., Robinson, C.J., Sahl, J.W., Stres, B., Thallinger, G.G., van Horn, D.J. & Weber, C.F. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 75377541.Google Scholar
Skotnicki, M.L., Selkirk, P.M., Broady, P., Adam, K.D. & Ninham, J.A. 2001. Dispersal of the moss Campylopus pyriformis on geothermal ground near the summits of Mount Erebus and Mount Melbourne, Victoria Land, Antarctica. Antarctic Science, 13, 280285.Google Scholar
Soo, R.M., Wood, S.A., Grzymski, J.J., McDonald, I.R. & Cary, S.C. 2009. Microbial biodiversity of thermophilic communities in hot mineral soils of Tramway Ridge, Mount Erebus, Antarctica. Environmental Microbiology, 11, 715728.Google Scholar
Sun, Y., Cai, Y.P., Liu, L., Yu, F.H., Farrell, M.L., McKendree, W. & Farmerie, W. 2009. ESPRIT: estimating species richness using large collections of 16S rRNA pyrosequences. Nucleic Acids Research, 37, 10.1093/nar/gkp285.CrossRefGoogle ScholarPubMed
Takami, H., Noguchi, H., Takaki, Y., Uchiyama, I., Toyoda, A., Nishi, S., Chee, G.J., Arai, W., Nunoura, T., Itoh, T., Hattori, M. & Takai, K. 2012. A deeply branching thermophilic bacterium with an ancient acetyl-CoA pathway dominates a subsurface ecosystem. PLoS One, 7, 10.1371/journal.pone.0030559.Google Scholar
Tiao, G., Lee, C.K., McDonald, I.R., Cowan, D.A. & Cary, S.C. 2012. Rapid microbial response to the presence of an ancient relic in the Antarctic Dry Valleys. Nature Communications, 3, 10.1038/ncomms1645.Google Scholar
Vanbreem, N. & Wielemak, W.G. 1974. Buffer intensities and equilibrium pH of minerals and soils. 1. Contribution of minerals and aqueous carbonate to pH buffering. Soil Science Society of America Journal, 38, 5560.CrossRefGoogle Scholar