An oligarchic microbial assemblage in the anoxic bottom waters of a volcanic subglacial lake

ISME Journal - Tập 3 Số 4 - Trang 486-497 - 2009
Eric Gaidos1,2, V. Marteinsson3, Þorsteinn Thorsteinsson4, Tómas Jøhannesson5, Árni Rafn Rúnarsson3, Andri Stefánsson6, S. A. Soule7, Brian Lanoil8, Mark Skidmore9, Sukkyun Han8, Mary Miller10, Antje Rusch1, W. Foo8
1Department of Geology and Geophysics, University of Hawaii at Manoa, Honolulu, HI, USA
2NASA Astrobiology Institute , Mountain View, CA , USA
3MATIS-Prokaria , Reykjavík , Iceland
4Hydrological Service, National Energy Authority , Reykjavík , Iceland
5Icelandic Meteorological Office, Reykjavík, Iceland
6Science Institute, University of Iceland, Reykjavík, Iceland
7Department of Oceanography, University of Hawaii, Honolulu, HI, USA
8Department of Environmental Sciences, University of California at Riverside , Riverside, CA , USA
9Department of Earth Sciences, Montana State University, Bozeman, MT, USA
10Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, USA

Tóm tắt

Abstract In 2006, we sampled the anoxic bottom waters of a volcanic lake beneath the Vatnajökull ice cap (Iceland). The sample contained 5 × 105 cells per ml, and whole-cell fluorescent in situ hybridization (FISH) and PCR with domain-specific probes showed these to be essentially all bacteria, with no detectable archaea. Pyrosequencing of the V6 hypervariable region of the 16S ribosomal RNA gene, Sanger sequencing of a clone library and FISH-based enumeration of four major phylotypes revealed that the assemblage was dominated by a few groups of putative chemotrophic bacteria whose closest cultivated relatives use sulfide, sulfur or hydrogen as electron donors, and oxygen, sulfate or CO2 as electron acceptors. Hundreds of other phylotypes are present at lower abundance in our V6 tag libraries and a rarefaction analysis indicates that sampling did not reach saturation, but FISH data limit the remaining biome to <10–20% of all cells. The composition of this oligarchy can be understood in the context of the chemical disequilibrium created by the mixing of sulfidic lake water and oxygenated glacial meltwater.

Từ khóa


Tài liệu tham khảo

Acinas, 2004, Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons, J Bacteriol, 186, 2629, 10.1128/JB.186.9.2629-2635.2004

Ágústsdóttir, 1994, Volatile fluxes integrated over four decades at Grímsvötn volcano, Iceland, J Geophys Res, 99, 9505, 10.1029/93JB03597

Aragno, 1998, Microbial Ecology, 79

Ashelford, 2002, PRIMROSE: a computer program for generating and estimating the phylogenetic range of 16S rRNA oligonucleotide probes and primers in conjunction with the RDP-II database, Nucleic Acids Res, 30, 3481, 10.1093/nar/gkf450

Bach, 2003, Iron and sulfide oxidation within the basaltic ocean crust: implications for chemolithoautotrophic microbial biomass production, Geochim Cosmochim Acta, 67, 3871, 10.1016/S0016-7037(03)00304-1

Balch, 1979, Methanogens: reevaluation of a unique biological group, Microbiol Rev, 43, 260, 10.1128/mr.43.2.260-296.1979

Behrens, 2001, Toxilogical and ecotoxilogical assessment of water tracers, Hydrogeol J, 9, 321, 10.1007/s100400100126

Behrens, 2003, In situ accessibility of small-subunit rRNA of members of the domains Bacteria, Archaea, and Eukarya to Cy3-labeled oligonucleotide probes, Appl Environ Microbiol, 69, 1748, 10.1128/AEM.69.3.1748-1758.2003

Björnsson, 2002, Subglacial lakes and jökulhlaups in Iceland, Glob Planet Change, 35, 255, 10.1016/S0921-8181(02)00130-3

Brinkmeyer, 2004, Predominance of β-proteobacteria in summer melt ponds on Arctic pack ice, Limnol Oceanogr, 49, 1013, 10.4319/lo.2004.49.4.1013

Brüggemann, 2003, The genome sequence of Clostridium tetani, the causative agent of tetanus disease, Proc Natl Acad Sci USA, 100, 1316, 10.1073/pnas.0335853100

Chapelle, 2002, A hydrogen-based subsurface microbial community dominated by methanogens, Nature, 415, 312, 10.1038/415312a

Chaturvedi, 2006, Exiguobacterium indicum sp. nov., a psychrophilic bacterium from the Hamta glacier of the Himalayan mountain ranges of India, Int J Syst Evol Microbiol, 56, 2765, 10.1099/ijs.0.64508-0

Chung, 2000, Thermus igniterrae sp. nov. and Thermus antranikianii sp. nov., two new species from Iceland, Int J Syst Evol Microbiol, 50, 209, 10.1099/00207713-50-1-209

Conrad, 1986, Thermodynamics of H2-consuming and H2-producing metabolic reactions in diverse methanogenic environments under in situ conditions, FEMS Microbiol Ecol, 38, 353, 10.1111/j.1574-6968.1986.tb01748.x

D’Imperio, 2008, Relative importance of H2 and H2S as energy sources for primary production in geothermal springs, Appl Environ Microbiol, 74, 5802, 10.1128/AEM.00852-08

Daims, 1999, Probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set, Syst Appl Microbiol, 22, 434, 10.1016/S0723-2020(99)80053-8

Drobner, 1992, Thiobacillus plumbophilus sp. nov., a novel galena and hydrogen oxidizer, Arch Microbiol, 157, 213, 10.1007/BF00245152

Engel, 2004, Bacterial diversity and ecosystem function of filamentous microbial mats from aphotic (cave) sulfidic springs dominated by chemolithoautotrophic ‘Epsilonproteobacteria’, Appl Environ Microbiol, 51, 31

Farr, 2004, Terrestrial analogs to Mars: The NRC community decadal report, Planet Space Sci, 52, 3, 10.1016/j.pss.2003.08.004

Finneran, 2003, Rhodoferax ferrireducens sp. nov. a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III), Int J Syst Evol Microbiol, 53, 669, 10.1099/ijs.0.02298-0

Frühling, 2002, Exiguobacterium tundrae sp. nov. and Exiguobacterium antarcticum sp. nov, Int J Syst Evol Microbiol, 52, 1171

Gaidos, 2007, A simple sampler for subglacial water bodies, J Glaciol, 53, 157, 10.3189/172756507781833820

Gaidos, 2004, A viable microbial community in a subglacial volcanic crater lake, Iceland, Astrobiology, 4, 327, 10.1089/ast.2004.4.327

Gaidos, 1999, Life in ice-covered oceans, Science, 284, 1631, 10.1126/science.284.5420.1631

Hoehler, 1999, Acetogenesis from CO2 in an anoxic marine sediment, Limnol Oceanogr, 44, 662, 10.4319/lo.1999.44.3.0662

Holmer, 2001, Sulphate reduction and sulphur cycling in lake sediments: a review, Freshwater Biol, 46, 431, 10.1046/j.1365-2427.2001.00687.x

Hugenholtz, 2001, Investigation of candidate division TM7, a recently recognized major lineage of the domain Bacteria with no known pure-culture representatives, Appl Environ Microbiol, 67, 411, 10.1128/AEM.67.1.411-419.2001

Huse, 2008, Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing, PLoS Genet, 4, e1000255, 10.1371/journal.pgen.1000255

Jensen, 1999, Effects of rhodamine water tracer on Escherichia coli densities, Water Res, 23, 257, 10.1016/0043-1354(89)90051-1

Jóhannesson, 2007, Circulation and thermodynamics in a subglacial geothermal lake under the Western Skaftá cauldron of the Vatnajökull ice cap, Iceland, Geophys Res Lett, 34, L19502, 10.1029/2007GL030686

Karr, 2006, Biodiversity of methanogenic and other Archaea in the permanently frozen Lake Fryxell, Antarctica, Appl Environ Microbiol, 72, 1663, 10.1128/AEM.72.2.1663-1666.2006

Kodama, 2004, Sulfuricurvum kujiense gen. nov., sp. nov., a facultatively anaerobic, chemolithoautotrophic, sulfur-oxidizing bacterium isolated from an underground crude-oil storage cavity, Int J Syst Evol Microbiol, 54, 2297, 10.1099/ijs.0.63243-0

Koschorreck, 2008, Microbial sulphate reduction at a low pH, FEMS Microbiol, 64, 329, 10.1111/j.1574-6941.2008.00482.x

Kotsyurbenko, 2001, Competition between homoacetogenic bacteria and methanogenic archaea for hydrogen at low temperature, FEMS Microbiol Ecol, 38, 153, 10.1111/j.1574-6941.2001.tb00893.x

Kotsyurbenko, 1995, New species of psychrophilic acetogens: Acetobacterium bakii sp. nov., A. paludosum sp. nov., A. fimetarium sp. nov, Arch Microbiol, 163, 29, 10.1007/BF00262200

Kuever, 2005, Bergey's Manual of Systematic Bacteriology, 988, 10.1007/0-387-29298-5_240

Lam, 2004, Processing deep-sea particle-rich water samples for fluorescence in situ hybridization: consideration of storage effects, preservations, and sonication, Appl Environ Microbiol, 70, 25, 10.1128/AEM.70.1.25-33.2004

Loy, 2007, probeBase—an online resource for rRNA-targeted oligonucleotide probes: new features 2007, Nucleic Acids Res, 35, D800, 10.1093/nar/gkl856

Luijten, 2003, Description of Sulfurospirillum halorespirans sp. nov., an anaerobic, tetrachloroethene-respiring bacterium, and transfer of Dehalospirillum multivorans to genus Sulfurospirillum as Sulfurospirillum multivorans comb, Int J Syst Evol Microbiol, 53, 787, 10.1099/ijs.0.02417-0

Macalady, 2008, Niche differentiation among sulfur-oxidizing bacterial populations in cave waters, ISME J, 2, 590, 10.1038/ismej.2008.25

Marteinsson, 2001, Phylogenetic diversity analysis of subterranean hot springs in Iceland, Appl Environ Microbiol, 67, 4242, 10.1128/AEM.67.9.4242-4248.2001

Marteinsson, 2001, Discovery and description of giant submarine smectite cones on the seafloor of Eyjafjordu, northern Iceland, and a novel thermal microbial habitat, Appl Environ Microbiol, 67, 827, 10.1128/AEM.67.2.827-833.2001

Methé, 1998, Contrasts between marine and freshwater bacterial community composition: analyses of communities in Lake George and six other Adirondack lakes, Limnol Oceanogr, 43, 368, 10.4319/lo.1998.43.2.0368

Millero, 2005, Chemical Oceanography, 10.1201/9780429258718

Nevin, 2005, Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates, Int J Syst Evol Microbiol, 55, 1667, 10.1099/ijs.0.63417-0

Pasternack, 1997, Volcanic lake systematics I. Physical constraints, Bull Volcanol, 58, 528, 10.1007/s004450050160

Peduzzi, 2003, Isolation and characterization of aggregate-forming sulfate-reducing and purple sulfur bacteria from the chemocline of meromictic Lake Cadagno, Switzerland, FEMS Microbiol Ecol, 45, 29, 10.1016/S0168-6496(03)00107-7

Priscu, 1999, Geomicrobiology of subglacial ice above Lake Vostok, Antarctica, Science, 286, 2141, 10.1126/science.286.5447.2141

Pruesse, 2007, SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB, Nucleic Acids Res, 35, 7188, 10.1093/nar/gkm864

Rainey, 1996, Clostridium paradoxum DSM 7308T contains multiple 16S rRNA genes with heterogeneous intervening sequences, Microbiology, 142, 2087, 10.1099/13500872-142-8-2087

Raskin, 1994, Group-specific 16S rRNA hybridization probes to describe natural communities of methanogens, Appl Environ Microbiol, 60, 1232, 10.1128/aem.60.4.1232-1240.1994

Rodrigues, 2006, Characterization of Exiguobacterium isolates from the Siberian permafrost. Description of Exiguobacterium sibericum sp. nov, Extremophiles, 10, 285, 10.1007/s00792-005-0497-5

Rodrigues, 2006, Multi-locus real-time PCR for quantitation of bacteria in the environment reveals Exiguobacterium to be prevalent in permafrost, FEMS Microbiol Ecol, 59, 489, 10.1111/j.1574-6941.2006.00233.x

Rozen, 2000, Bioinformatics Methods and Protocols: Methods in Molecular Biology, 365

Sadeghifard, 2006, The mosaic nature of intergenic 16S-23S rRNA spacer regions suggests rRNA operon copy number variation in Clostridium difficile strains, Appl Environ Microbiol, 72, 7311, 10.1128/AEM.01179-06

Sheridan, 2003, Phylogenetic analysis of anaerobic psychrophilic enrichment cultures obtained from a Greenland glacier ice core, Appl Environ Microbiol, 69, 2153, 10.1128/AEM.69.4.2153-2160.2003

Siegert, 2005, A revised inventory of Antarctic subglacial lakes, Antarct Sci, 17, 453, 10.1017/S0954102005002889

Skidmore, 2005, Comparison of microbial community compositions of two subglacial environments reveals a possible role for microbes in chemical weathering processes, Appl Environ Microbiol, 71, 6986, 10.1128/AEM.71.11.6986-6997.2005

Skírnisdóttir, 2000, Influence of sulfide and temperature on species composition and community structure of hot spring microbial mats, Appl Environ Microbiol, 66, 2835, 10.1128/AEM.66.7.2835-2841.2000

Skírnisdóttir, 2001, Isolation and characterization of a mixotrophic sulfur-oxidizing Thermus scotoductus, Extremophiles, 5, 45, 10.1007/s007920000172

Sogin, 2006, Microbial diversity in the deep sea and the underexplored ‘rare biosphere’, Proc Natl Acad Sci USA, 103, 12115, 10.1073/pnas.0605127103

Spear, 2005, Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem, Proc Natl Acad Sci USA, 102, 2555, 10.1073/pnas.0409574102

Stackebrandt, 1997, Phylogenetic analysis of the genus Desulfotomaculum: evidence for the misclassification of Desulfotomaculum guttoideum and description of Desulfotomatculum orientis as Desulfosporosinus orientis gen. nov., comb. nov, Int J Syst Bacteriol, 47, 1134, 10.1099/00207713-47-4-1134

Stahl, 1991, Nucleic Acid Techniques in Bacterial Systematics, 205

Thorsteinsson, 2008, A hot water drill with built-in sterilization: design, testing, and performance, Jökull, 51, 71

Ueki, 2006, Paludibacter propionicigenes gen. nov., sp. nov., a novel strictly anaerobic, Gram-negative, propionate-producing bacterium isolated from plant residue in irrigated rice-field soil in Japan, Int J Syst Evol Microbiol, 56, 39, 10.1099/ijs.0.63896-0

Wang, 2007, Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy, Appl Environ Microbiol, 73, 5261, 10.1128/AEM.00062-07