Phylogenetic and functional analysis of metagenome sequence from high-temperature archaeal habitats demonstrate linkages between metabolic potential and geochemistry

Frontiers in Microbiology

Volumn 4, Issue MAY, 2013, Pages

  Inskeep, William P ^a   Jay, Zackary J ^a   Herrgard, Markus J ^b   Kozubal, Mark A ^a   Rusch, Douglas B ^c   Tringe, Susannah G ^d   Macur, Richard E ^a   Jennings, Ryan de M ^a   Boyd, Eric S ^a   Spear, John R ^e   Roberto, Francisco F ^f  

^a MONTANA STATE UNIVERSITY   (United States)

^b Chalmers University of Technology   (Denmark)

^c INDIANA UNIVERSITY   (United States)

^d DOE JOINT GENOME INSTITUTE   (United States)

^e Department of Geology and Geological Engineering   (United States)

^f a wholly owned subsidiary of Newmont Mining Corporation   (United States)

Author keywords

Archaea; Functional genomics; Geochemistry; Phylogeny; Thermophilic archaea and bacteria

Indexed keywords

ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; DNA EXTRACTION; ELECTRON TRANSPORT; GAS CHROMATOGRAPHY; GEOCHEMISTRY; KINETICS; METAGENOME; MICROBIAL COMMUNITY; NONHUMAN; OXIDATION REDUCTION REACTION; PH; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; TEMPERATURE; THAUMARCHAEOTA; VIRUS GENOME;

ARCHAEA;

EID: 84884273235     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00095     Document Type: Article

References (100)

1. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
2. Amend, J. P., and Shock, E. L. (2001). Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol. Rev. 25, 175-243.
3. Auchtung, T. A., Shyndriayeva, G., and Cavanaugh, C. M. (2011). 16S rRNA phylogenetic analysis and quantification of Korarchaeota indigenous to the hot springs of Kamchatka, Russia. Extremophiles 15, 105-116.
4. Auernik, K. S., and Kelly, R. M. (2008). Identification of components of electron transport chains in the extremely thermoacidophilic crenarchaeon Metallosphaera sedula through iron and sulfur compound oxidation transcriptomes. Appl. Environ. Microbiol. 74, 7723-7732.
5. Auguet, J. C., Barberan, A., and Casamayor, E. O. (2009). Global ecological patterns in uncultured Archaea. ISME J. 4, 182-190.
6. Badger, J. H., Hoover, T. R., Brun, Y. V., Weiner, R. M., Laub, M. T., Alexandre, G., et al. (2006). Comparative genomic evidence for a close relationship betwÎn the dimorphic prosthecate bacteria Hyphomonas neptunium and Caulobacter crescentus. J. Bacteriol. 188, 6841-6850.
7. Ball, J. W., Nordstrom, D. K., Cunningham, K. M., Schoonen, M. A. A., Xu, Y., and DeMonge, J. M. (1998). Water-Chemistry and Onsite Sulfur Speciation Data for Selected Springs in Yellowstone National Park, Wyoming, 1994-1995. U.S. Geological Survey Open-File Report 98-574, Boulder, CO.
8. Ball, J. W., McCleskey, R. B., Nordstrom, D. K., Holloway, J. M., and Verplanck, P. L. (2002). Water-Chemistry Data for Selected Springs, Geysers, and Streams in Yellowstone National Park, Wyoming 1999-2000. U.S. Geological Survey Open File Report 02-382, Boulder, CO.
9. Barnes, S. M., Fundyga, R. E., Jeffries, M. W., and Pace, N. R. (1994). Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. Proc. Natl. Acad. Sci. U.S.A. 91, 1609-1613.
10. Bathe, S., and Norris, P. R. (2007). Ferrous iron- and sulfur-induced genes in Sulfolobus metallicus. Appl. Environ. Microbiol. 73, 2491-2497.
11. Beam, J. P., Jay, Z. J., Kozubal, M. A., and Inskeep, W.P. (2011). "Distribution and ecology of thaumarchaea in geothermal environments," in The 11th International Conference on Thermophiles Research, September 11-16 (Big Sky: Thermophiles). [Abstr. PA-009].
12. Berg, I. A., Kockelkorn, D., Buckel, W., and Fuchs, G. (2007). A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318, 1782-1786.
13. Berg, I. A., Ramos-Vera, W. H., Petri, A., Huber, H., and Fuchs, G. (2010a). Study of the distribution of autotrophic CO2 fixation cycles in Crenarchaeota. Microbiology 156, 256-269.
14. Berg, I. A., Kockelkorn, D., Ramos-Vera, W. H., Say, R. F., Zarzycki, J., Hügler, M., et al. (2010b). Autotrophic carbon fixation in archaea. Nat. Rev. Microbiol. 8, 447-460.
15. Blumentals, I. I., Itoh, M., Olson, G. J., and Kelly, R. M. (1990). Role of polysulfides in reduction of elemental sulfur by the hyperthermophilic archaebacterium Pyrococcus furiosus. Appl. Environ. Microbiol. 56, 1255-1262.
16. Boyd, E. S., Jackson, R. A., Encarnacion, G., Zahn, J. A., Beard, T., Leavitt, W. D., et al. (2007). Isolation, characterization, and ecology of sulfur-respiring Crenarchaea inhabiting acid-sulfate-chloride geothermal springs in Yellowstone National Park. Appl. Environ. Microbiol. 73, 6669-6677.
17. Brierley, C. L., and Brierley, J. A. (1973). A chemoautotrophic and thermophilic microorganism isolated from an acid hot spring. Can. J. Microbiol. 19, 183-188.
18. Brochier-Armanet, C., Boussau, B., Gribaldo, S., and Forterre, P. (2008). Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245-252.
19. Brock, T. D., Brock, K. M., Belly, R. T., and Weiss, R. L. (1972). Sulfolobus: a new genus of sulfur-oxidizing bacteria living at low pH and high temperature. Arch. Mikrobiol. 84, 54-68.
20. Casanueva, A., Galada, N., Baker, G. C., Grant, W. D., Heaphy, S., Jones, B., et al. (2008). Nanoarchaeal 16S rRNA gene sequences are widely dispersed in hyperthermophilic and mesophilic halophilic environments. Extremophiles 12, 651-656.
21. Chaban, B., Ng, S. Y., and Jarrell, K. F. (2006). Archaeal habitats - from the extreme to the ordinary. Can. J. Microbiol. 52, 73-116.
22. Cherney, M. M., Zhang, Y., Solomonsona, M., Weinera, J. H., and James, N. G. (2010). Crystal Structure of Sulfide:quinone oxidoreductase from Acidithiobacillus ferrooxidans: insights into sulfidotrophic respiration and detoxification. J. Mol. Biol. 398, 292-305.
23. Clingenpeel, S., Kan, J., Macur, R. E., Lovalvo, D., Varley, J., Inskeep, W. P., et al. (2011). "Yellowstone lake reveals evidence of non-extreme Nanoarchaeota and ecotype diversity," in The 11th International Conference on Thermophiles Research, September 11-16 (Big Sky: Thermophiles). [Abstr. PA-079].
24. Das, A., Silaghi-Dumitrescu, R., Ljungdahl, L. G., and Kurtz, D. M. (2005). Cytochrome bd oxidase, oxidative stress, and dioxygen tolerance of the strictly anaerobic bacterium Moorella thermoacetica. J. Bacteriol. 187, 2020-2029.
25. de la Torre, J. R., Walker, C. B., Ingalls, A. E., Könneke, M., and Stahl, D. A. (2008). Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ. Microbiol. 10, 810-818.
26. DeLong, E. F. (2005). Microbial community genomics in the ocean. Nat. Rev. Microbiol. 3, 459-469.
27. Dhillon, A., Lever, M., Lloyd, K. G., Albert, D. B., Sogin, M. L., and Teske, A. (2005). Methanogen diversity evidenced by molecular characterization of methyl coenzyme M reductase A (mcrA) genes in hydrothermal sediments of the Guaymas Basin. Appl. Environ. Microbiol. 71, 4592-4601.
28. Eddy, S. R. (2011). Accelerated profile HMM searches. PLoS Comput. Biol. 7:e1002195. doi:10.1371/journal.pcbi.1002195
29. Elkins, J. G., Kunin, V., Anderson, I., Barry, K., Goltsman, E., Podar, M., et al. (2008). A korarchaeal genome reveals new insights into the evolution of the Archaea. Proc. Natl. Acad. Sci. U.S.A. 105, 8102-8107.
30. Ettwig, K. F., Speth, D. R., Reimann, J., Wu, M. L., Jetten, M. S. M., and Keltjens, J. T. (2012). Bacterial oxygen production in the dark. Front. Microbiol. 3:273. doi:10.3389/fmicb.2012.00273
31. Falkowski, P. G., Fenchel, T., and Delong, E. F. (2008). The microbial engines that drive Earth's biogeochemical cycles. Science 23, 1034-1039.
32. Ferry, J. G. (1999). Enzymology of one-carbon metabolism in methanogenic pathways. FEMS Microbiol. Rev. 23, 13-38.
33. Fitz-Gibbon, S. T., Ladner, H., Kim, U. J., Stetter, K. O., Simon, M. I., and Miller, J. H. (2002). Genome sequence of the hyperthermophilic crenarchaeon Pyrobaculum aerophilum. Proc. Natl. Acad. Sci. U.S.A. 99, 984-989.
34. Flock, U., Watmough, N. J., and Ädelroth, P. (2005). Electron/proton coupling in bacterial nitric oxide reductase during reduction of oxygen. Biochemistry 44, 10711-10719.
35. Friedrich, C. G., Bardischewsky, F., Rother, D., Quentmeier, A., and Fischer, J. (2005). Prokaryotic sulfur oxidation. Curr. Opin. Microbiol. 8, 253-259.
36. García-Horsman, J. A., Barquera, B., Rumbley, J., Ma, J., and Gennis, R. B. (1994). The superfamily of heme-copper respiratory oxidases. J. Bacteriol. 176, 5587-5600.
37. Ghosh, W., and Dam, B. (2009). Biochemistry and molecular biology of lithotrophic sulfur oxidation by taxonomically and ecologically diverse bacteria and archaea. FEMS Microbiol. Rev. 33, 999-1043.
38. González, P. J., Correia, C., Moura, I., Brondino, C. D., and Moura, J. J. (2006). Bacterial nitrate reductases: molecular and biological aspects of nitrate reduction. J. Inorg. Biochem. 100, 1015-1023.
39. Grissa, I., Vergnaud, G., and Pourcel, C. (2007). CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 35(Suppl. 2), W52-W57.
40. Hamamura, N., Macur, R. E., Korf, S., Ackerman, G., Taylor, W. P., Kozubal, M. A., et al. (2009). Linking microbial oxidation of arsenic with detection and phylogenetic analysis of arsenite-oxidase genes in diverse geothermal environments. Environ. Microbiol. 11, 421-431.
41. Hatzenpichler, R., Lebedeva, E. V., Spieck, E., Stoecker, K., Richter, A., Daims, H., et al. (2008). A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc. Natl. Acad. Sci. U.S.A. 105, 2134-2139.
42. Hedderich, R., Hamann, N., and Bennati, M. (2005). Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster. Biol. Chem. 386, 961-970.
43. Hohn, M. J., Hedlund, B. P., and Huber, H. (2002). Detection of 16S rDNA sequences representing the novel phylum "Nanoarchaeota": indication for a world-wide distribution in high temperature biotopes. Syst. Appl. Microbiol. 25, 551-554.
44. Huber, H., Gallenberger, M., Jahn, U., Eylert, E., Berg, I. A., Kockelkorn, D., et al. (2008). A dicarboxylate/4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis. Proc. Natl. Acad. Sci. U.S.A. 105, 7851-7856.
45. Huber, H., Hohn, M. J., Rachel, R., Fuchs, T., Wimmer, V. C., and Stetter, K. O. (2002). A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63-67.
46. Huber, H., Huber, R., and Stetter, K. O. (2006). "Thermoproteales," in The Prokaryotes, eds M. Dworkin, S. Falkow, E. Rosenberg, K.-H. Schleifer, and E. Stackebrandt (New York: Springer), 10-22.
47. Hügler, M., Krieger, R. S., Jahn, M., and Fuchs, G. (2003). Characterization of acetyl-CoA/propionyl-CoA carboxylase in Metallosphaera sedula: carboxylating enzyme in the 3-hydroxypropionate cycle for autotrophic carbon fixation. Eur. J. Biochem. 270, 736-744.
48. Inskeep, W. P., Ackerman, G. G., Taylor, W. P., Kozubal, M. A., Korf, S., and Macur, R. E. (2005). On the energetics of chemolithotrophy: case studies of geothermal springs in Yellowstone National Park. Geobiology 3, 297-317.
49. Inskeep, W. P., Jay, Z. J., Tringe, S. G., Herrgard, M., Rusch, D. B., et al. (2013). The YNP metagenome project: environmental parameters responsible for microbial distribution in the Yellowstone geothermal ecosystem. Front. Microbiol. 4:67. doi:10.3389/fmicb.2013.00067
50. Inskeep, W. P., Macur, R. E., Harrison, G., Bostick, B. C., and Fendorf, S. (2004). Biomineralization of As(V)-hydrous ferric oxyhydroxide mats in an acid-sulfate-chloride geothermal spring of Norris Geyser Basin, Yellowstone National Park. Geochim. Cosmochim. Acta 68, 3141-3155.
51. Inskeep, W. P., Rusch, D. B., Jay, Z. J., Herrgard, M. J., Kozubal, M. A., Richardson, T. H., et al. (2010). Metagenomes from high-temperature chemotrophic systems reveal geochemical controls on microbial community structure and function. PLoS ONE 5:e9773. doi:10.1371/journal.pone.0009773
52. Itoh, T., Suzuki, K., and Nakase, T. (2002). Vulcanisaeta distributa gen. nov., sp nov., and Vulcanisaeta souniana sp nov., novel hyperthermophilic rod-shaped crenarchaeotes isolated from hot springs in Japan. Int. J. Syst. Evol. Microbiol. 52, 1097-1104.
53. Itoh, T., Suzuki, K., Sanchez, P. C., and Nakase, T. (1999). Caldivirga maquilingensis gen. nov., sp nov., a new genus of rod-shaped crenarchaeote isolated from a hot spring in the Philippines. Int. J. Syst. Bacteriol. 49, 1157-1163.
54. Jahn, U., Huber, H., Eisenreich, W., Hugler, M., and Fuchs, L. (2007). Insights into the autotrophic CO2 fixation pathway of the archaeon Ignicoccus hospitalis: comprehensive analysis of the central carbon metabolism. J. Bacteriol. 189, 4108-4119.
55. Jay, Z. J., Planer-Friedrich, B., Rusch, D. B., and Inskeep, W. P. (2011). "Linking geochemistry to microbial community structure and function in sulfidic geothermal systems of Yellowstone National Park," in Goldschmidt Conference, August 2011, Prague, CR. Mineralogical Magazine 75, 1104.
56. Kozubal, M., Macur, R. E., Korf, S., Taylor, W. P., Ackerman, G. G., Nagy, A., et al. (2008). Isolation and distribution of a novel iron-oxidizing crenarchaeon from acidic geothermal springs in Yellowstone National Park. Appl. Environ. Microbiol. 74, 942-949.
57. Kozubal, M. A., Dem Jennings, R., Jay, Z., Beam, J. P., Tringe, S. G., Rusch, D. B., et al. (2013). Geoarchaeota: a new Candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park. ISME J. 7, 622-634.
58. Kozubal, M. A., Dlakic, M., Macur, R. E., and Inskeep, W. P. (2011). Terminal oxidase diversity and function in "Metallosphaera yellowstonensis": gene expression and protein modeling suggest mechanisms of Fe(II) oxidation in the sulfolobales. Appl. Environ. Microbiol. 77, 1844-1853.
59. Kozubal, M. A., Macur, R. E., Jay, Z. J., Beam, J. P., Malfatti, S. A., Tringe, S. G., et al. (2012). Microbial iron cycling in acidic geothermal springs of Yellowstone National Park: integrating molecular surveys, geochemical processes and isolation of novel Fe-active microorganisms. Front. Microbiol. 3:109. doi:10.3389/fmicb.2012.00109
60. Langner, H. W., Jackson, C. R., McDermott, T. R., and Inskeep, W. P. (2001). Rapid oxidation of arsenite in a hot spring ecosystem, Yellowstone National Park. Environ. Sci. Technol. 35, 3302-3309.
61. Laska, S., Lottspeich, F., and Kletzin, A. (2003). Membrane-bound hydrogenase and sulfur reductase of the hyperthermophilic and acidophilic archaeon Acidianus ambivalens. Microbiology 149, 2357-2371.
62. Li, M., Chen, Z., Zhang, P., Pan, X., Jiang, C., An, X., et al. (2008). Crystal structure studies on sulfur oxygenase reductase from Acidianus tengchongensis. Biochem. Biophys. Res. Commun. 369, 919-923.
63. Macur, R. E., Jay, Z. J., Taylor, W. P., Kozubal, M. A., Kocar, B. D., and Inskeep, W. P. (2013). Microbial community structure and sulfur biogeochemistry in mildly-acidic sulfidic geothermal springs in Yellowstone National Park. Geobiology 11, 86-99.
64. Macur, R. E., Langner, H. W., Kocar, B. D., and Inskeep, W. P. (2004). Linking geochemical processes with microbial community analysis: successional dynamics in an arsenic-rich, acid-sulfate-chloride geothermal spring. Geobiology 2, 163-177.
65. Makarova, K. S., Aravind, L., Wolf, Y. I., and Koonin, E. V. (2011). Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol. Direct 6, 38.
66. Mardanov, A. V., Svetlitchnyi, V. A., Beletsky, A. V., Prokofeva, M. I., Bonch-Osmolovskaya, E. A., Ravin, N. V., et al. (2010). The genome sequence of the crenarchaeon Acidilobus saccharovorans supports a new order, Acidilobales, and suggests an important ecological role in terrestrial acidic hot springs. Appl. Environ. Microbiol. 76, 5652-5657.
67. Markowitz, V. M., Chen, I.-M. A., Chu, K., Szeto, E., Palaniappan, K., Grechkin, Y., et al. (2012). IMG/M: the integrated metagenome data management and comparative analysis system. Nucleic Acids Res. 40, D123-D129.
68. McCleskey, R. B., Ball, J. W., Nordstrom, D. K., Holloway, J. M., and Taylor, H. E. (2005). Water-Chemistry Data for Selected Hot Springs, Geysers, and Streams in Yellowstone National Park, Wyoming 2001-2002. United States Geological Survey Open File Report 2004-1316, Boulder, CO.
69. Meyer-Dombard, D., Shock, E. L., and Amend, J. P. (2005). Archaeal and bacterial communities in geochemically diverse hot springs of Yellowstone National Park, USA. Geobiology 3, 211-227.
70. Miller-Coleman, R. L., Dodsworth, J. A., Ross, C. A., Shock, E. L., Williams, A. J., Hartnett, H. E., et al. (2012). Korarchaeota diversity, biogeography, and abundance in Yellowstone and Great Basin Hot Springs and ecological niche modeling based on machine learning. PLoS ONE 7:e35964. doi:10.1371/journal.pone.0035964
71. Nordstrom, D. K., Ball, J. W., and McClesky, R. B. (2005). "Geothermal water to surface water: chemistry of thermal outflows in Yellowstone National Park," in Geothermal Biology and Geochemistry in Yellowstone National Park, eds W. P. Inskeep, and T. R. McDermott (Bozeman, MT: Thermal Biology Institute), 73-94.
72. Parks, D. H., and Beiko, R. G. (2010). Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26, 715-721.
73. Pester, M., Schleper, C., and Wagner, M. (2011). The Thaumarchaeota: an emerging view of their phylogeny and ecophysiology. Curr. Opin. Microbiol. 14, 300-306.
74. Prokofeva, M. I., Kostrikina, N. A., Kolganova, T. V., Tourova, T. P., Lysenko, A. M., Lebedinsky, A. V., et al. (2009). Isolation of the anaerobic thermoacidophilic crenarchaeote Acidilobus saccharovorans sp. nov. and proposal of Acidilobales ord. nov., including Acidilobaceae fam. nov. and Caldisphaeraceae fam. nov. Int. J. Syst. Evol. Microbiol. 59, 3116-3122.
75. Quatrini, R., Appia-Ayme, C., Denis, Y., Jedlicki, E., Holmes, D. S., and Bonnefoy, V. (2009). Extending the models for iron and sulfur oxidation in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics 10:394. doi:10.1186/1471-2164-10-394
76. Ramos-Vera, W. H., Berg, I. A., and Fuchs, G. (2009). Autotrophic carbon dioxide assimilation in Thermoproteales revisited. J. Bacteriol. 191, 4286-4297.
77. Ramos-Vera, W. H., Weiss, M., Strittmatter, E., Kockelkorn, D., and Fuchs, G. (2011). Identification of missing genes and enzymes for autotrophic carbon fixation in Crenarchaeota. J. Bact. 193, 1201-1211.
78. Rhee, S.-K., and Fuchs, G. (1999). Phenylacetyl-CoA:acceptor oxidoreductase, a membrane-bound molybdenum-iron-sulfur enzyme involved in anaerobic metabolism of phenylalanine in the denitrifying bacterium Thauera aromatic. Eur. J. Biochem. 262, 507-515.
79. Rice, G., Stedman, K., Snyder, J., Wiedenheft, B., Willits, D., Brumfield, S., et al. (2001). Viruses from extreme thermal environments. Proc. Natl. Acad. Sci. U.S.A. 98, 13341-13345.
80. Rusch, D. B., Halpern, A. L., Sutton, G., Heidelberg, K. B., Williamson, S., Yooseph, S., et al. (2007). The sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol. 5:e77. doi:10.1371/journal.pbio.0050077
81. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., et al. (2003). A free, open-source system for microarray data management and analysis. BioTechniques 34, 374-378.
82. Schleper, C., Jurgens, G., and Jonuscheit, M. (2005). Genomic studies of uncultivated archaea. Nat. Rev. Microbiol. 3, 479-488.
83. Schut, G. J., Bridger, S. L., and Adams, M. W. W. (2007). Insights into the metabolism of elemental sulfur by the hyperthermophilic archaeon Pyrococcus furiosus: characterization of a coenzyme A-dependent NAD(P)H sulfur-oxidoreductase. J. Bacteriol. 189, 4431-4441.
84. Segerer, A., Langworthy, T. A., and Stetter, K. O. (1988). Thermoplasma acidophilum and Thermoplasma volcanium sp-nov from solfatara fields. Syst. Appl. Microbiol. 10, 161-171.
85. Selengut, J. D., Haft, D. H., Davidsen, T., Ganapathy, A., Gwinn-Giglio, M., Nelson, W. C., et al. (2007). TIGRFAMs and genome properties: tools for the assignment of molecular function and biological process in prokaryotic genomes. Nucleic Acids Res. 35, D260-D264.
86. Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., et al. (2010). Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol. 18, 331-340.
87. Spear, J. R., Walker, J. J., McCollom, T. M., and Pace, N. R. (2005). Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem. Proc. Natl. Acad. Sci. U.S.A. 102, 2555-2560.
88. Stetter, K. O. (2006). History of discovery of the first hyperthermophiles. Extremophiles 10, 357-362.
89. Takacs-Vesbach, C., Inskeep, W. P., Jay, Z. J., Herrgard, M., Rusch, D. B., Tringe, S. G., et al. (2013). Metagenome sequence analysis of filamentous microbial communities obtained from geochemically distinct geothermal channels reveals specialization of three Aquificales lineages. Front. Microbiol. 4:84. doi:10.3389/fmicb.2013.0084
90. Teeling, H., Meyerdierks, A., Bauer, M., Amann, R., and Glöckner, F. O. (2004). Application of tetranucleotide frequencies for the assignment of genomic fragments. Environ. Microbiol. 6, 938-947.
91. Viginais, P. M., and Billoud, B. (2007). Occurrence, classification and biological function of hydrogenases. Chem. Rev. 107, 4206-4272.
92. Volkl, P., Huber, R., Drobner, E., Rachel, R., Burggraf, S., Trincone, A., et al. (1993). Pyrobaculum aerophilum sp. nov., a novel nitrate-reducing hyperthermophilic archaeum. Appl. Environ. Microbiol. 59, 2918-2926.
93. Walker, C. B., de la Torre, J. R., Klotz, M. G., Urakawa, H., Pinel, N., Arp, D. J., et al. (2010). Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. U.S.A. 107, 8818-8823.
94. Waters, E., Hohn, M. J., Ahel, I., Graham, D. E., Adams, M. D., Barnstead, M., et al. (2003). The genome of Nanoarchaeum equitans: insights into early archaeal evolution and derived parasitism. Proc. Natl. Acad. Sci. U.S.A. 100, 12984-12988.
95. Watmough, N. J., Field, S. J., Hughes, R. J., and Richardson, D. J. (2009). The bacterial respiratory nitric oxide reductase. Biochem. Soc. Trans. 37, 392-399.
96. Woese, C. R., and Fox, G. E. (1977). Phylogenetic structure of the prokaryotic domains: the primary kingdoms. Proc. Natl. Acad. Sci. U.S.A. 74, 5088-5090.
97. Woese, C. R., Kandler, O., and Wheelis, M. L. (1990). Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl. Acad. Sci. U.S.A. 87, 4576-4579.
98. Xu, Y., Schoonen, M. A. A., Nordstrom, D. K., Cunningham, K. M., and Ball, J. W. (1998). Sulfur geochemistry of hydrothermal waters in Yellowstone National Park: I. The origin of thiosulfate in hot spring waters. Geochim. Cosmochim. Acta 62, 3729-3743.
99. Xu, Y., Schoonen, M. A. A., Nordstrom, D. K., Cunningham, K. M., and Ball, J. W. (2000). Sulfur geochemistry of hydrothermal waters in Yellowstone National Park, Wyoming, USA. II. Formation and decomposition of thiosulfate and polythionate in Cinder Pool. J. Volcanol. Geotherm. Res. 97, 407-423.
100. Young, M., Wiedenheft, B., Snyder, J., Spuhler, J., Roberto, F., and Douglas, T. (2005). "Archaeal viruses from Yellowstone's high-temperature environments," in Geothermal Biology and Geochemistry in YNP, eds W. P. Inskeep, and T. R. McDermott (Bozeman, MT: Montana State University Publications), 289-304.