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Archaeal diversity revealed in Antarctic sea ice

Published online by Cambridge University Press:  25 May 2011

Rebecca O.M. Cowie
Affiliation:
School of Biological Sciences, Victoria University of Wellington, Wellington 6010, New Zealand National Institute of Water and Atmospheric Research (NIWA), Greta Point, Wellington, New Zealand
Elizabeth W. Maas
Affiliation:
National Institute of Water and Atmospheric Research (NIWA), Greta Point, Wellington, New Zealand
Ken G. Ryan*
Affiliation:
School of Biological Sciences, Victoria University of Wellington, Wellington 6010, New Zealand
*
*author for correspondence: [email protected]

Abstract

Archaea, once thought to be only extremophiles, are now known to be abundant in most environments. They can predominate in microbial communities and be significantly involved in many global biogeochemical cycles. However, Archaea have not been reported in Antarctic sea ice. Our understanding of the ecology of Antarctic sea ice prokaryotes is still in its infancy but this information is important if we are to understand their diversity, adaptations and biogeochemical roles in Antarctic systems. We detected Archaea in sea ice at two sampling sites taken from three subsequent years using conserved 16S rRNA gene archaeal primers and PCR. Archaeal abundance was measured using quantitative PCR and community diversity was investigated by sequencing cloned 16S rRNA gene PCR products. Archaea in Antarctic sea ice were found to be in low abundance consisting of ≤ 6.6% of the prokaryotic community. The majority, 90.8% of the sequences, clustered with the recently described phylum Thaumarchaeota, one group closely clustered with the ammonia-oxidizing Candidatus Nitrosopumilus maritimus. The remainder of the clones grouped with the Euryarchaeota.

Type
Biological Sciences
Copyright
Copyright © Antarctic Science Ltd 2011

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References

Arrigo, K.R.Thomas, D.N. 2004. Large-scale importance of sea ice biology in the Southern Ocean. Antarctic Science, 16, 471486.CrossRefGoogle Scholar
Ashelford, K.E., Chuzhanova, N., Fry, J.C., Jones, A.J.Weightman, A.J. 2005. At least one in twenty 16S rRNA sequence records currently held in public repositories estimated to contain substantial anomalies. Applied and Environmental Microbiology, 71, 77247736.CrossRefGoogle Scholar
Bano, N., Ruffin, S., Ransom, B.Hollibaugh, J.T. 2004. Phylogenetic composition of Arctic Ocean archaeal assemblages and comparison with Antarctic assemblages. Applied and Environmental Microbiology, 70, 781789.CrossRefGoogle ScholarPubMed
Barns, S.M., Fundyga, R.E., Jeffries, M.W.Pace, N.R. 1994. Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. PNAS, 91, 16091613.CrossRefGoogle Scholar
Bowman, J.P., McCammon, S.A., Brown, J.L., Nichols, D.S.McMeekin, T.A. 1997. Diversity and association of psychrophilic Bacteria in Antarctic sea ice. Applied and Environmental Microbiology, 63, 16011609.CrossRefGoogle ScholarPubMed
Brinkmeyer, R., Knittel, K., Jürgens, J., Weyland, H., Amann, R.Helmke, E. 2003. Diversity and structure of bacterial communities in Arctic versus Antarctic pack ice. Applied and Environmental Microbiology, 69, 66106619.CrossRefGoogle ScholarPubMed
Brochier-Armanet, C., Boussau, B., Gribaldo, S.Forterre, P. 2008. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nature Reviews in Microbiology, 6, 245252.CrossRefGoogle ScholarPubMed
Brown, M.V.Bowman, J.P. 2001. A molecular phylogenetic survey of sea ice microbial communities SIMCO. FEMS Microbiology Ecology, 35, 267275.CrossRefGoogle ScholarPubMed
Church, M.J., DeLong, E.F., Ducklow, H.W., Karner, M.B., Preston, C.M.Karl, D.M. 2003. Abundance and distribution of planktonic archaea and bacteria in the waters west of the Antarctic Peninsula. Limnology and Oceanography, 48, 18931902.CrossRefGoogle Scholar
Cole, J.R., Chai, B., Marsh, T.L., Farris, R.J., Wang, Q., Kulam, S.A. et al. 2003. The Ribosomal Database Project RDPII: previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Research, 31, 442443.CrossRefGoogle ScholarPubMed
Collins, R.E., Rocap, G.Deming, J.W. 2010. Persistence of bacterial and archaeal communities in sea ice through an Arctic winter. Environmental Microbiology, 12, 18281841.CrossRefGoogle ScholarPubMed
Delille, D. 1992. Marine bacterioplankton at the Weddell Sea ice edge, distribution of psychrophilic and psychrotrophic populations. Polar Biology, 12, 205210.CrossRefGoogle Scholar
DeLong, E.F. 1992. Archaea in coastal marine environments. PNAS, 89, 56855689.CrossRefGoogle ScholarPubMed
DeLong, E.F., Wu, K.Y., Prezelin, B.B.Jovine, R.V.M. 1994. High abundance of Archaea in Antarctic marine picoplankton. Nature, 371, 69697.CrossRefGoogle ScholarPubMed
Deming, J.W. 2002. Psychrophiles and polar regions. Current Opinions in Microbiology, 5, 301309.CrossRefGoogle ScholarPubMed
Elkins, J.G., Podarc, M., Graham, D.E., Makarovae, K.S., Wolfe, Y. et al. 2008. A korarchaeal genome reveals insights into the evolution of the Archaea. PNAS, 105, 81028107.CrossRefGoogle ScholarPubMed
Evans, C.A., O'Reilly, J.E.Thomas, J.P. 1987. A handbook for the measurement of chlorophyll a and primary production. College Station, TX: Texas A&M University, 114 pp.Google Scholar
Felsenstein, J. 1989. PHYLIP - Phylogeny Inference Package, version 3.2. Cladistics, 5, 164166.Google Scholar
Franzmann, P.D., Stackebrandt, E., Sanderson, K., Volkman, J.K., Cameron, D.E., Stevenson, P.L., McMeekin, T.A.Burton, H.R. 1988. Halobacterium lacusprofundi sp. nov, a halophilic bacterium isolated from Deep Lake, Antarctica. Systematic and Applied Microbiology, 11, 207.CrossRefGoogle Scholar
Fuhrman, J.A., Hewson, I., Schwalbach, M.S., Steele, J.A., Brown, M.V.Naeem, S. 2006. Annually reoccurring bacterial communities are predictable from ocean conditions. PNAS, 103, 13 10413 109.CrossRefGoogle ScholarPubMed
Gillan, D.C.Danis, B. 2007. The archaebacterial communities in Antarctic bathypelagic sediments. Deep-Sea Research II, 54, 16821690.CrossRefGoogle Scholar
Hooker, J.D. 1847. The botany of the Antarctic voyage of H.M. Discovery ships Erebus and Terror in the years 1838–1843. Part 1. Flora Antarctica. London: Reeve Brothers.Google Scholar
Howard-Williams, C., Peterson, D., Lyons, W.B., Cattaneo-Vietti, R.Gordon, S. 2006. Measuring ecosystem response in a rapidly changing environment, the Latitudinal Gradient Project. Antarctic Science, 18, 465471.CrossRefGoogle Scholar
Huber, H., Hohn, M.J., Rachel, R., Fuchs, T., Wimmer, V.C.Stetter, K.O. 2002. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature, 417, 6367.CrossRefGoogle ScholarPubMed
Huson, D.H., Richter, D.C., Rausch, C., Dezulian, T., Franz, M.Rupp, R. 2007. Dendroscope: an interactive viewer for large phylogenetic trees. BMC Bioinformatics, 8, 460.CrossRefGoogle ScholarPubMed
Jukes, T.H.Cantor, C.R. 1969. Evolution of protein molecules. In Munro, H., ed. Mammalian protein metabolism, vol. 3. New York: Academic Press, 2132.CrossRefGoogle Scholar
Junge, K., Eicken, H.Deming, J.W. 2004. Bacterial activity at -2 to -20 degrees C in Arctic wintertime sea ice. Applied and Environmental Microbiology, 70, 550557.CrossRefGoogle ScholarPubMed
Kalanetra, K.M., Bano, N.Hollibaugh, J.T. 2009. Ammonia oxidizing Archaea in the Arctic Ocean and Antarctic coastal waters. Environmental Microbiology, 11, 24342445.CrossRefGoogle ScholarPubMed
Karner, M.B., Delong, E.F.Karl, D.M. 2001. Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature, 409, 507510.CrossRefGoogle ScholarPubMed
Karr, E.A., Ng, J.M., Belchik, S.M., Sattley, W.M., Madigan, M.T.Achenbach, L.A. 2006. Biodiversity of methanogenic and other Archaea in the permanently frozen Lake Fryxell, Antarctica. Applied and Environmental Microbiology, 72, 16631666.CrossRefGoogle ScholarPubMed
Konneke, M., Bernhard, A.E., de la Torre, J.R., Walker, C.B., Waterbury, J.B.Stahl, D.A. 2005. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature, 437, 543546.CrossRefGoogle ScholarPubMed
Lane, D.J. 1991. 16S/23S rRNA Sequencing. In Stackebrandt, E. & Goodfellow, M., ed. Nucleic acid techniques in bacterial systematics. Chichester: John Wiley, 115175.Google Scholar
Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G.W., Prosser, J.I., Schuster, S.C.Schleper, C. 2006. Archaea predominate among ammonia oxidizing prokaryotes in soils. Nature, 442, 807809.CrossRefGoogle ScholarPubMed
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H. et al. 2004. ARB, a software environment for sequence data. Nucleic Acids Research, 32, 13631371.CrossRefGoogle ScholarPubMed
Martin, A., Hall, J.A., O'Toole, R., Davy, S.K.Ryan, K.G. 2008. High single cell metabolic activity in Antarctic sea ice bacteria. Aquatic Microbial Ecology, 52, 2531.CrossRefGoogle Scholar
Massana, R., Delong, E.F.Pedros-Alio, C. 2000. A few cosmopolitan phylotypes dominate planktonic archaeal assemblages in widely different oceanic provinces. Applied and Environmental Microbiology, 66, 17771787.CrossRefGoogle ScholarPubMed
McMinn, A., Ryan, K.G., Ralph, P.J.Pankowshi, A. 2007. Spring sea ice photosynthesis, primary production and biomass distribution in eastern Antarctica, 2002–2004. Marine Biology, 151, 985999.CrossRefGoogle Scholar
Mock, T.Thomas, D.N. 2005. Recent advances in sea ice microbiology. Environmental Microbiology, 7, 605619.CrossRefGoogle ScholarPubMed
Moeseneder, M.M., Winter, C., Arrieta, J.M.Herndl, G.J. 2001. Terminal restriction fragment length polymorphism (TRFLP) screening of a marine archaeal library to determine the different phylotypes. Journal of Microbiological Methods, 44, 159172.CrossRefGoogle ScholarPubMed
Murray, A.E.Grzymski, J.J. 2007. Diversity and genomics of Antarctic marine microorganisms. Philosophical Transactions of the Royal Society, B362, 22592271.CrossRefGoogle Scholar
Murray, A.E., Wu, K.Y., Moyer, C.L., Karl, D.M.DeLong, E.F. 1999. Evidence for circumpolar distribution of planktonic Archaea in the Southern Ocean. Aquatic Microbial Ecology, 18, 263273.CrossRefGoogle Scholar
Murray, A.E., Preston, C.M., Massana, R., Taylor, L.T., Blakis, A., Wu, K.DeLong, E.F. 1998. Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Applied and Environmental Microbiology, 64, 25852595.CrossRefGoogle ScholarPubMed
Preston, C.M., Wu, K., Molinski, T.F.DeLong, E.F. 1996. A psychrophilic crenarchaeon inhabits a marine sponge: Cenarcheum symbiosis gen. nov., sp. nov. PNAS, 93, 62416246.CrossRefGoogle ScholarPubMed
Ryan, K.G., Ralph, P.Mcminn, A. 2004. Acclimation of Antarctic bottom-ice algal communities to lowered salinities during melting. Polar Biology, 27, 679686.CrossRefGoogle Scholar
Ryan, K.G., Cowie, R.O.M., Liggins, L., McNaughtan, D., Martin, A.Davy, S.K. 2009. The short-term effect of irradiance on the photosynthetic properties of Antarctic fast-ice microalgae communities. Journal of Phycology, 45, 12901298.CrossRefGoogle Scholar
Stein, J.L.Simon, M.I. 1996. Archaeal ubiquity. PNAS, 93, 62286230.CrossRefGoogle ScholarPubMed
Wells, L.E.Deming, J.W. 2003. Abundance of bacteria, the Cytophaga–Flavobacterium cluster and Archaea in cold oligotrophic waters and nepheloid layers of the Northwest Passage, Canadian Archipelago. Aquatic Microbial Ecology, 31, 1931.CrossRefGoogle Scholar
Woese, C.R., Kandler, O.Wheelis, M.L. 1990. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. PNAS, 87, 45764579.CrossRefGoogle ScholarPubMed