Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota

International Journal of Systematic and Evolutionary Microbiology

Volumn 64, Issue PART 8, 2014, Pages 2738-2752

  Stieglmeier, Michaela ^a   Klingl, Andreas ^b   Alves, Ricardo J E ^a   Rittmann, Simon K M R ^a   Melcher, Michael ^a   Leisch, Nikolaus ^a   Schleper, Christa ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; CARBON DIOXIDE; PYRUVIC ACID; RNA 16S;

AEROBIC BACTERIUM; AMMONIA OXIDIZING ARCHAEON; ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL STRAIN; BACTERIUM ISOLATE; CRENARCHAEOTA; DNA BASE COMPOSITION; ELECTRON MICROSCOPY; EURYARCHAEOTA; KORARCHAEOTA; MESOPHILIC BACTERIUM; NITROSOSPHAERA VIENNENSIS; NONHUMAN; PHYLUM; PRIORITY JOURNAL; RNA SEQUENCE; SOIL; SULFOLOBALES; TEMPERATURE; THAUMARCHAEOTA; TYPE STRAIN;

AMMONIA; AUSTRIA; BASE COMPOSITION; CRENARCHAEOTA; DNA, ARCHAEAL; GLYCERYL ETHERS; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SOIL MICROBIOLOGY;

EID: 84906069307     PISSN: 14665026     EISSN: None     Source Type: Journal    
DOI: 10.1099/ijs.0.063172-0     Document Type: Article

References (143)

1. Adair, K. L. & Schwartz, E. (2008). Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of northern Arizona, USA. Microb Ecol 56, 420-426.
2. Alonso-Sáez, L., Waller, A. S., Mende, D. R., Bakker, K., Farnelid, H., Yager, P. L., Lovejoy, C., Tremblay, J. E., Potvin, M. & other authors (2012). Role for urea in nitrification by polar marine archaea. Proc Natl Acad Sci U S A 109, 17989-17994.
3. Alves, R. J. E., Wanek, W., Zappe, A., Richter, A., Svenning, M. M., Schleper, C. & Urich, T. (2013). Nitrification rates in Arctic soils are associated with functionally distinct populations of ammoniaoxidizing archaea. ISME J 7, 1620-1631.
4. Amano, F. & Noda, T. (1995). Improved detection of nitric oxide radical (NO.) production in an activated macrophage culture with a radical scavenger, carboxy PTIO and Griess reagent. FEBS Lett 368, 425-428.
5. Andrews, S. C., Robinson, A. K. & Rodríguez-Quiñones, F. (2003). Bacterial iron homeostasis. FEMS Microbiol Rev 27, 215-237.
6. Arp, D. J. & Stein, L. Y. (2003). Metabolism of inorganic N compounds by ammonia-oxidizing bacteria. Crit Rev Biochem Mol Biol 38, 471-495.
7. Bates, S. T., Berg-Lyons, D., Caporaso, J. G., Walters, W. A., Knight, R. & Fierer, N. (2011). Examining the global distribution of dominant archaeal populations in soil. ISME J 5, 908-917.
8. Baumeister, W. & Lembcke, G. (1992). Structural features of archaebacterial cell envelopes. J Bioenerg Biomembr 24, 567-575.
9. Berg, I. A., Kockelkorn, D., Buckel, W. & Fuchs, G. (2007). A3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. Science 318, 1782-1786.
10. Blainey, P. C., Mosier, A. C., Potanina, A., Francis, C. A. & Quake, S. R. (2011). Genome of a low-salinity ammonia-oxidizing archaeon determined by single-cell and metagenomic analysis. PLoS ONE 6, e16626.
11. Box, G. E. P. & Draper, N. R. (1987). Empirical Model-Building and Response Surfaces. Oxford: Wiley.
12. Box, G. E. P. & Lucas, H. L. (1959). Design of experiments in nonlinear situations. Biometrika 46, 77-90.
13. Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. (2008). Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6, 245-252.
14. Brochier-Armanet, C., Forterre, P. & Gribaldo, S. (2011). Phylogeny and evolution of the Archaea: one hundred genomes later. Curr Opin Microbiol 14, 274-281.
15. Collingridge, P. W. & Kelly, S. (2012). MergeAlign: improving multiple sequence alignment performance by dynamic reconstruction of consensus multiple sequence alignments. BMC Bioinformatics 13, 117.
16. de la Torre, J. R., Walker, C. B., Ingalls, A. E., Könneke, M. & Stahl, D. A. (2008). Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 10, 810-818.
17. Deatherage, J. F., Taylor, K. A. & Amos, L. A. (1983). Threedimensional arrangement of the cell wall protein of Sulfolobus acidocaldarius. J Mol Biol 167, 823-848.
18. DeLong, E. F. (1992). Archaea in coastal marine environments. Proc Natl Acad Sci U S A 89, 5685-5689.
19. DeLong, E. F., Wu, K. Y., Prézelin, B. B. & Jovine, R. V. M. (1994). High abundance of archaea in Antarctic marine picoplankton. Nature 371, 695-697.
20. Derringer, G. & Suich, R. (1980). Simultaneous optimization of several response variables. J Qual Technol 12, 214-219.
21. Di, H. J., Cameron, K. C., Shen, J. P., Winefield, C. S., O'Callaghan, M., Bowatte, S. & He, J. Z. (2009). Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nat Geosci 2, 621-624.
22. Di Tommaso, P., Moretti, S., Xenarios, I., Orobitg, M., Montanyola, A., Chang, J. M., Taly, J. F. & Notredame, C. (2011). T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 39(Web Server issue), W13-W17.
23. Dridi, B., Fardeau, M.-L., Ollivier, B., Raoult, D. & Drancourt, M. (2012). Methanomassiliicoccus luminyensisgen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. Int J Syst Evol Microbiol 62, 1902-1907.
24. Durbin, A. M. & Teske, A. (2010). Sediment-associated microdiversity within the marine group I Crenarchaeota. Environ Microbiol Rep 2, 693-703.
25. Edgar, R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792-1797.
26. Eichler, J. (2003). Facing extremes: archaeal surface-layer (glyco)proteins. Microbiology 149, 3347-3351.
27. Elkins, J. G., Podar, M., Graham, D. E., Makarova, K. S., Wolf, Y., Randau, L., Hedlund, B. P., Brochier-Armanet, C., Kunin, V. & other authors (2008). A korarchaeal genome reveals insights into the evolution of the Archaea. Proc Natl Acad Sci U S A 105, 8102-8107.
28. Eme, L., Reigstad, L. J., Spang, A., Lanzén, A., Weinmaier, T., Rattei, T., Schleper, C. & Brochier-Armanet, C. (2013). Metagenomics of Kamchatkan hot spring filaments reveal two new major (hyper)thermophilic lineages related to Thaumarchaeota. Res Microbiol 164, 425-438.
29. Erbilgin, O., McDonald, K. L. & Kerfeld, C. A. (2014). Characterization of a planctomycetal organelle: a novel bacterial microcompartment for the aerobic degradation of plant saccharides. Appl Environ Microbiol 80, 2193-2205.
30. Erguder, T. H., Boon, N., Wittebolle, L., Marzorati, M. & Verstraete, W. (2009). Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev 33, 855-869.
31. Ettwig, K. F., van Alen, T., van de Pas-Schoonen, K. T., Jetten, M. S. M. & Strous, M. (2009). Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol 75, 3656-3662.
32. Fernandez-Castillo, R., Rodriguez-Valera, F., Gonzalez-Ramos, J. & Ruiz-Berraquero, F. (1986). Accumulation of poly(b-hydroxybutyrate) by halobacteria. Appl Environ Microbiol 51, 214-216.
33. Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E. & Oakley, B. B. (2005). Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci U S A 102, 14683-14688.
34. French, E., Kozlowski, J. A., Mukherjee, M., Bullerjahn, G. & Bollmann, A. (2012). Ecophysiological characterization of ammonia-oxidizing archaea and bacteria from freshwater. Appl Environ Microbiol 78, 5773-5780.
35. Fuhrman, J. A., McCallum, K. & Davis, A. A. (1992). Novel major archaebacterial group from marine plankton. Nature 356, 148-149.
36. Gordon, D. A. & Giovannoni, S. J. (1996). Detection of stratified microbial populations related toChlorobiumandFibrobacterspecies in the Atlantic and Pacific oceans. Appl Environ Microbiol 62, 1171-1177.
37. Grogan, D. W. (1996). Organization and interactions of cell envelope proteins of the extreme thermoacidophileSulfolobus acidocaldarius. Can J Microbiol 42, 1163-1171.
38. Gubry-Rangin, C., Nicol, G. W. & Prosser, J. I. (2010). Archaea rather than bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74, 566-574.
39. Haikarainen, T. & Papageorgiou, A. C. (2010). Dps-like proteins: structural and functional insights into a versatile protein family. Cell Mol Life Sci 67, 341-351.
40. Hallam, S. J., Konstantinidis, K. T., Putnam, N., Schleper, C., Watanabe, Y., Sugahara, J., Preston, C., de la Torre, J., Richardson, P. M. & DeLong, E. F. (2006a). Genomic analysis of the uncultivated marine crenarchaeoteCenarchaeum symbiosum. Proc Natl Acad Sci U S A 103, 18296-18301.
41. Hallam, S. J., Mincer, T. J., Schleper, C., Preston, C. M., Roberts, K., Richardson, P. M. & DeLong, E. F. (2006b). Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marineCrenarchaeota. PLoS Biol 4, e95.
42. Hatzenpichler, R. (2012). Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78, 7501-7510.
43. 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. Proc Natl Acad Sci U S A 105, 2134-2139.
44. He, J. Z., Shen, J. P., Zhang, L. M., Zhu, Y. G., Zheng, Y. M., Xu, M. G. & Di, H. (2007). Quantitative analyses of the abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea of a Chinese upland red soil under long-term fertilization practices. Environ Microbiol 9, 2364-2374.
45. Hershberger, K. L., Barns, S. M., Reysenbach, A. L., Dawson, S. C. & Pace, N. R. (1996). Wide diversity of Crenarchaeota. Nature 384, 420.
46. Hooper, A. B. & Terry, K. R. (1979). Hydroxylamine oxidoreductase of Nitrosomonas. Production of nitric oxide from hydroxylamine. Biochim Biophys Acta 571, 12-20.
47. Horak, R. E. A., Qin, W., Schauer, A. J., Armbrust, E. V., Ingalls, A. E., Moffett, J. W., Stahl, D. A. & Devol, A. H. (2013). Ammonia oxidation kinetics and temperature sensitivity of a natural marine community dominated by Archaea. ISME J 7, 2023-2033.
48. Huber, H., Burggraf, S., Mayer, T., Wyschkony, I., Rachel, R. & Stetter, K. O. (2000). Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophicArchaea, represented by two new species, Ignicoccus islandicussp. nov. andIgnicoccus pacificus sp. nov. Int J Syst Evol Microbiol 50, 2093-2100.
49. 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, 63-67.
50. Hugenholtz, P., Pitulle, C., Hershberger, K. L. & Pace, N. R. (1998). Novel division level bacterial diversity in a Yellowstone hot spring. J Bacteriol 180, 366-376.
51. Jarrell, K. F. & Albers, S.-V. (2012). The archaellum: an old motility structure with a new name. Trends Microbiol 20, 307-312.
52. Jia, Z. & Conrad, R. (2009). Bacteriarather than Archaeadominate microbial ammonia oxidation in an agricultural soil. Environ Microbiol 11, 1658-1671.
53. Jorgensen, S. L., Hannisdal, B., Lanzén, A., Baumberger, T., Flesland, K., Fonseca, R., Ovreås, L., Steen, I. H., Thorseth, I. H. & other authors (2012). Correlating microbial community profiles with geochemical data in highly stratified sediments from the Arctic MidOcean Ridge. Proc Natl Acad Sci U S A 109, E2846-E2855.
54. Jung, M. Y., Park, S. J., Min, D., Kim, J. S., Rijpstra, W. I. C., Sinninghe Damsté, J. S., Kim, G. J., Madsen, E. L. & Rhee, S. K. (2011). Enrichment and characterization of an autotrophic ammoniaoxidizing archaeon of mesophilic crenarchaeal group I. 1a from an agricultural soil. Appl Environ Microbiol 77, 8635-8647.
55. Jurgens, G., Lindström, K. & Saano, A. (1997). Novel group within the kingdom Crenarchaeota from boreal forest soil. Appl Environ Microbiol 63, 803-805.
56. Kallmeyer, J., Pockalny, R., Adhikari, R. R., Smith, D. C. & D'Hondt, S. (2012). Global distribution of microbial abundance and biomass in subseafloor sediment. Proc Natl Acad Sci U S A 109, 16213-16216.
57. Karner, M. B., DeLong, E. F. & Karl, D. M. (2001). Archaeal dominance in the mesopelagic zone of the Pacific Ocean. Nature 409, 507-510.
58. Katoh, K. & Toh, H. (2010). Parallelization of theMAFFTmultiple sequence alignment program. Bioinformatics 26, 1899-1900.
59. Katoh, K., Kuma, K., Toh, H. & Miyata, T. (2005). MAFFTversion 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33, 511-518.
60. Kim, B. K., Jung, M. Y., Yu, D. S., Park, S. J., Oh, T. K., Rhee, S. K. & Kim, J. F. (2011). Genome sequence of an ammonia-oxidizing soil archaeon, "CandidatusNitrosoarchaeum koreensis" MY1. J Bacteriol 193, 5539-5540.
61. Klingl, A. (2011). Struktur und Funktion von S-Layern acidophiler Bakterien und Archaeen, ihre Rolle bei der Pyrit-Oxidation sowie die Adhäsion an Oberflächen. Dissertation, University of Regensburg, Regensburg, Germany.
62. Klingl, A., Moissl-Eichinger, C., Wanner, G., Zweck, J., Huber, H., Thomm, M. & Rachel, R. (2011). Analysis of the surface proteins of Acidithiobacillus ferrooxidans strain SP5/1 and the new, pyriteoxidizingAcidithiobacillusisolate HV2/2, and their possible involvement in pyrite oxidation. Arch Microbiol 193, 867-882.
63. Klingl, A., Flechsler, J., Heimerl, T. & Rachel, R. (2013). Archaeal cells. IneLS. Chichester: Wiley.
64. König, H., Rachel, R. & Claus, H. (2007). Proteinaceous surface layers of archaea: ultrastructure and biochemistry. In Archaea: Molecular and Cellular Biology, pp. 315-340. Edited by R. Cavicchioli. Washington, DC: American Society for Microbiology.
65. Könneke, 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, 543-546.
66. Lane, D. J., Pace, B., Olsen, G. J., Stahl, D. A., Sogin, M. L. & Pace, N. R. (1985). Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci U S A 82, 6955-6959.
67. Lehtovirta-Morley, L. E., Stoecker, K., Vilcinskas, A., Prosser, J. I. & Nicol, G. W. (2011). Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc Natl Acad Sci U S A 108, 15892-15897.
68. 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, 806-809.
69. Leisch, N., Dirks, U., Gruber-Vodicka, H. R., Schmid, M., Sterrer, W. & Ott, J. A. (2011). Microanatomy of the trophosome region of Paracatenulacf. polyhymnia (Catenulida, Platyhelminthes) and its intracellular symbionts. Zoomorphology 130, 261-271.
70. Lembcke, G., Dürr, R., Hegerl, R. & Baumeister, W. (1991). Image analysis and processing of an imperfect two-dimensional crystal: the surface layer of the archaebacterium Sulfolobus acidocaldarius reinvestigated. J Microsc 161, 263-278.
71. Lembcke, G., Baumeister, W., Beckmann, E. & Zemlin, F. (1993). Cryo-electron microscopy of the surface protein of Sulfolobus shibatae. Ultramicroscopy 49, 397-406.
72. Lindsay, M. R., Webb, R. I., Strous, M., Jetten, M. S., Butler, M. K., Forde, R. J. & Fuerst, J. A. (2001). Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. Arch Microbiol 175, 413-429.
73. MacGregor, B. J., Moser, D. P., Alm, E. W., Nealson, K. H. & Stahl, D. A. (1997). Crenarchaeota in Lake Michigan sediment. Appl Environ Microbiol 63, 1178-1181.
74. Marcy, Y., Ouverney, C., Bik, E. M., Lösekann, T., Ivanova, N., Martin, H. G., Szeto, E., Platt, D., Hugenholtz, P. & other authors (2007). Dissecting biological "dark matter" with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc Natl Acad Sci U S A 104, 11889-11894.
75. Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R. & Stahl, D. A. (2009). Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461, 976-979.
76. Merbt, S. N., Stahl, D. A., Casamayor, E. O., Martí, E., Nicol, G. W. & Prosser, J. I. (2012). Differential photoinhibition of bacterial and archaeal ammonia oxidation. FEMS Microbiol Lett 327, 41-46.
77. Miller, M. A., Pfeiffer, W. & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Gateway Computing Environments Workshop (GCE) 2010, 14 November 2010, pp. 1-8. Chicago: IEEE.
78. Mosier, A. C., Allen, E. E., Kim, M., Ferriera, S. & Francis, C. A. (2012a). Genome sequence of "CandidatusNitrosoarchaeum limnia" BG20, a low-salinity ammonia-oxidizing archaeon from the San Francisco Bay estuary. J Bacteriol 194, 2119-2120.
79. Mosier, A. C., Allen, E. E., Kim, M., Ferriera, S. & Francis, C. A. (2012b). Genome sequence of "CandidatusNitrosopumilus salaria" BD31, an ammonia-oxidizing archaeon from the San Francisco Bay estuary. J Bacteriol 194, 2121-2122.
80. Muller, F., Brissac, T., Le Bris, N., Felbeck, H. & Gros, O. (2010). First description of giant archaea (Thaumarchaeota) associated with putative bacterial ectosymbionts in a sulfidic marine habitat. Environ Microbiol 12, 2371-2383.
81. Mussmann, M., Brito, I., Pitcher, A., Sinninghe Damsté, J. S., Hatzenpichler, R., Richter, A., Nielsen, J. L., Nielsen, P. H., Müller, A. & other authors (2011). Thaumarchaeotes abundant in refinery nitrifying sludges express amoA but are not obligate autotrophic ammonia oxidizers. Proc Natl Acad Sci U S A 108, 16771-16776.
82. Nicol, G. W. & Schleper, C. (2006). Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle? Trends Microbiol 14, 207-212.
83. Nunoura, T., Takaki, Y., Kakuta, J., Nishi, S., Sugahara, J., Kazama, H., Chee, G. J., Hattori, M., Kanai, A. & other authors (2011). Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res 39, 3204-3223.
84. Ochsenreiter, T., Selezi, D., Quaiser, A., Bonch-Osmolovskaya, L. & Schleper, C. (2003). Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5, 787-797.
85. Offre, P., Prosser, J. I. & Nicol, G. W. (2009). Growth of ammoniaoxidizing archaea in soil microcosms is inhibited by acetylene. FEMS Microbiol Ecol 70, 99-108.
86. Park, S. J., Kim, J. G., Jung, M. Y., Kim, S. J., Cha, I. T., Ghai, R., MartínCuadrado, A. B., Rodríguez-Valera, F. & Rhee, S. K. (2012). Draft genome sequence of an ammonia-oxidizing archaeon, "Candidatus Nitrosopumilus sediminis" AR2, from Svalbard in the Arctic Circle. J Bacteriol 194, 6948-6949.
87. Pelve, E. A., Lindås, A. C., Martens-Habbena, W., de la Torre, J. R., Stahl, D. A. & Bernander, R. (2011). Cdv-based cell division and cell cycle organization in the thaumarchaeonNitrosopumilus maritimus. Mol Microbiol 82, 555-566.
88. Pester, M., Rattei, T., Flechl, S., Gröngröft, A., Richter, A., Overmann, J., Reinhold-Hurek, B., Loy, A. & Wagner, M. (2012). amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoAgenes from soils of four different geographic regions. Environ Microbiol 14, 525-539.
89. Pitcher, A., Rychlik, N., Hopmans, E. C., Spieck, E., Rijpstra, W. I. C., Ossebaar, J., Schouten, S., Wagner, M. & Sinninghe Damsté, J. S. (2010). Crenarchaeol dominates the membrane lipids ofCandidatus Nitrososphaera gargensis, a thermophilic group I. 1b archaeon. ISME J 4, 542-552.
90. Preston, C. M., Wu, K. Y., Molinski, T. F. & DeLong, E. F. (1996). A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci U S A 93, 6241-6246.
91. Prosser, J. I. & Nicol, G. W. (2012). Archaeal and bacterial ammoniaoxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20, 523-531.
92. Prüschenk, R. & Baumeister, W. (1987). Three-dimensional structure of the surface protein ofSulfolobus solfataricus. Eur J Cell Biol 45, 185-191.
93. Prüschenk, R., Baumeister, W. & Zillig, W. (1987). Surface structure variants in different species ofSulfolobus. FEMS Microbiol Lett 43, 327-330.
94. Rachel, R., Pum, D., Šmarda, J., Šmajs, D., Komrska, J., Krzyzánek, V., Rieger, G. & Stetter, K. O. (1997). II. Fine structure of S-layers 1. FEMS Microbiol Rev 20, 13-23.
95. Rachel, R., Meyer, C., Klingl, A., Gürster, S., Heimerl, T., Wasserburger, N., Burghardt, T., Küper, U., Bellack, A. & other authors (2010). Analysis of the ultrastructure of archaea by electron microscopy. Methods Cell Biol 96, 47-69.
96. Rappé, M. S. & Giovannoni, S. J. (2003). The uncultured microbial majority. Annu Rev Microbiol 57, 369-394.
97. Reigstad, L. J., Richter, A., Daims, H., Urich, T., Schwark, L. & Schleper, C. (2008). Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 64, 167-174.
98. Rinke, C., Schwientek, P., Sczyrba, A., Ivanova, N. N., Anderson, I. J., Cheng, J. F., Darling, A., Malfatti, S., Swan, B. K. & other authors (2013). Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431-437.
99. Rittmann, S. & Herwig, C. (2012). A comprehensive and quantitative review of dark fermentative biohydrogen production. Microb Cell Fact 11, 115.
100. Santoro, A. E. & Casciotti, K. L. (2011). Enrichment and characterization of ammonia-oxidizing archaea from the open ocean: phylogeny, physiology and stable isotope fractionation. ISME J 5, 1796-1808.
101. Schauss, K., Focks, A., Leininger, S., Kotzerke, A., Heuer, H., ThieleBruhn, S., Sharma, S., Wilke, B. M., Matthies, M. & other authors (2009). Dynamics and functional relevance of ammonia-oxidizing archaea in two agricultural soils. Environ Microbiol 11, 446-456.
102. Schleper, C. & Nicol, G. W. (2010). Ammonia-oxidising archaea-physiology, ecology and evolution. Adv Microb Physiol 57, 1-41.
103. Schleper, C., Holben, W. & Klenk, H. P. (1997). Recovery of crenarchaeotal ribosomal DNA sequences from freshwater-lake sediments. Appl Environ Microbiol 63, 321-323.
104. Schmidt, T. M., DeLong, E. F. & Pace, N. R. (1991). Analysis of a marine picoplankton community by 16S rRNA gene cloning and sequencing. J Bacteriol 173, 4371-4378.
105. Schouten, S., Hopmans, E. C., Baas, M., Boumann, H., Standfest, S., Könneke, M., Stahl, D. A. & Sinninghe Damsté, J. S. (2008). Intact membrane lipids of "Candidatus Nitrosopumilus maritimus, " a cultivated representative of the cosmopolitan mesophilic group I Crenarchaeota. Appl Environ Microbiol 74, 2433-2440.
106. Shen, J. P., Zhang, L. M., Zhu, Y. G., Zhang, J. B. & He, J. Z. (2008). Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environ Microbiol 10, 1601-1611.
107. Shen, T. L., Stieglmeier, M., Dai, J. L., Urich, T. & Schleper, C. (2013). Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformisto nitrification inhibitors. FEMS Microbiol Lett 344, 121-129.
108. Shively, J. M., Ball, F., Brown, D. H. & Saunders, R. E. (1973). Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) ofThiobacillus neapolitanus. Science 182, 584-586.
109. Sinninghe Damsté, J. S., Schouten, S., Hopmans, E. C., van Duin, A. C. T. & Geenevasen, J. A. J. (2002). Crenarchaeol: the characteristic core glycerol dibiphytanyl glycerol tetraether membrane lipid of cosmopolitan pelagic crenarchaeota. J Lipid Res 43, 1641-1651.
110. Sinninghe Damsté, J. S., Rijpstra, W. I., Hopmans, E. C., Jung, M. Y., Kim, J. G., Rhee, S. K., Stieglmeier, M. & Schleper, C. (2012). Intact polar and core glycerol dibiphytanyl glycerol tetraether lipids of group I. 1a and I. 1b thaumarchaeota in soil. Appl Environ Microbiol 78, 6866-6874.
111. Sleytr, U. B., Messner, P., Pum, D. & Sára, M. (1993). Crystalline bacterial cell surface layers. Mol Microbiol 10, 911-916.
112. Sleytr, U. B., Sara, M., Pum, D. & Schuster, B. (2001). Characterization and use of crystalline bacterial cell surface layers. Prog Surf Sci 68, 231-278.
113. Sleytr, U. B., Huber, C., Ilk, N., Pum, D., Schuster, B. & Egelseer, E. M. (2007). S-layers as a tool kit for nanobiotechnological applications. FEMS Microbiol Lett 267, 131-144.
114. Spang, A., Hatzenpichler, R., Brochier-Armanet, C., Rattei, T., Tischler, P., Spieck, E., Streit, W., Stahl, D. A., Wagner, M. & Schleper, C. (2010). Distinct gene set in two different lineages of ammonia-oxidizing archaea supports the phylum Thaumarchaeota. Trends Microbiol 18, 331-340.
115. Spang, A., Poehlein, A., Offre, P., Zumbrägel, S., Haider, S., Rychlik, N., Nowka, B., Schmeisser, C., Lebedeva, E. V. & other authors (2012). The genome of the ammonia-oxidizingCandidatusNitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ Microbiol 14, 3122-3145.
116. Spang, A., Martijn, J., Saw, J. H., Lind, A. E., Guy, L. & Ettema, T. J. (2013). Close encounters of the third domain: the emerging genomic view of archaeal diversity and evolution. Archaea 2013, 202358.
117. Stahl, D. A. & de la Torre, J. R. (2012). Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66, 83-101.
118. Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688-2690.
119. Stamatakis, A., Hoover, P. & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57, 758-771.
120. Stein, J. L., Marsh, T. L., Wu, K. Y., Shizuya, H. & DeLong, E. F. (1996). Characterization of uncultivated prokaryotes: isolation and analysis of a 40-kilobase-pair genome fragment from a planktonic marine archaeon. J Bacteriol 178, 591-599.
121. Stieglmeier, M., Alves, R. J. E. & Schleper, C. (2014a). Thaumarchaeota. In The Prokaryotes, 4th edn. Edited by E. Rosenberg, E. F. DeLong, S. Lory, E. Stackebrandt & F. Thompson. Berlin & Heidelberg: Springer (in press).
122. Stieglmeier, M., Mooshammer, M., Kitzler, B., Wanek, W., Zechmeister-Boltenstern, S., Richter, A. & Schleper, C. (2014b). Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J 8, 1135-1146.
123. Takai, K., Moser, D. P., DeFlaun, M., Onstott, T. C. & Fredrickson, J. K. (2001). Archaeal diversity in waters from deep South African gold mines. Appl Environ Microbiol 67, 5750-5760.
124. Taylor, K. A., Deatherage, J. F. & Amos, L. A. (1982). Structure of the S-layer ofSulfolobus acidocaldarius. Nature 299, 840-842.
125. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
126. Tourna, M., Stieglmeier, M., Spang, A., Könneke, M., Schintlmeister, A., Urich, T., Engel, M., Schloter, M., Wagner, M. & other authors (2011). Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc Natl Acad Sci U S A 108, 8420-8425.
127. Treusch, A. H., Leininger, S., Kletzin, A., Schuster, S. C., Klenk, H. P. & Schleper, C. (2005). Novel genes for nitrite reductase and Amorelated proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 7, 1985-1995.
128. Tyson, G. W. & Banfield, J. F. (2005). Cultivating the uncultivated: a community genomics perspective. Trends Microbiol 13, 411-415.
129. Urakawa, H., Martens-Habbena, W. & Stahl, D. A. (2011). Physiology and genomics of ammonia-oxidizing archaea. In Nitrification, pp. 117-155. Edited by B. B. Ward, D. J. Arp & M. G. Klotz. Washington, DC: American Society for Microbiology.
130. Vajrala, N., Martens-Habbena, W., Sayavedra-Soto, L. A., Schauer, A., Bottomley, P. J., Stahl, D. A. & Arp, D. J. (2013). Hydroxylamine as an intermediate in ammonia oxidation by globally abundant marine archaea. Proc Natl Acad Sci U S A 110, 1006-1011.
131. Vallenet, D., Labarre, L., Rouy, Z., Barbe, V., Bocs, S., Cruveiller, S., Lajus, A., Pascal, G., Scarpelli, C. & Médigue, C. (2006). MaGe: a microbial genome annotation system supported by synteny results. Nucleic Acids Res 34, 53-65.
132. Vallenet, D., Engelen, S., Mornico, D., Cruveiller, S., Fleury, L., Lajus, A., Rouy, Z., Roche, D., Salvignol, G. & other authors (2009). MicroScope: a platform for microbial genome annotation and comparative genomics. Database (Oxford)2009, bap021.
133. van Niftrik, L. & Jetten, M. S. M. (2012). Anaerobic ammoniumoxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76, 585-596.
134. van Niftrik, L. A., Fuerst, J. A., Sinninghe Damsté, J. S., Kuenen, J. G., Jetten, M. S. M. & Strous, M. (2004). The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 233, 7-13.
135. Veith, A., Klingl, A., Zolghadr, B., Lauber, K., Mentele, R., Lottspeich, F., Rachel, R., Albers, S. V. & Kletzin, A. (2009). Acidianus, Sulfolobus andMetallosphaerasurface layers: structure, composition and gene expression. Mol Microbiol 73, 58-72.
136. Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., Wu, D., Paulsen, I., Nelson, K. E. & other authors (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66-74.
137. Walker, C. B., de la Torre, J. R., Klotz, M. G., Urakawa, H., Pinel, N., Arp, D. J., Brochier-Armanet, C., Chain, P. S. G., Chan, P. P. & other authors (2010). Nitrosopumilus maritimusgenome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci U S A 107, 8818-8823.
138. Whitman, W. B., Coleman, D. C. & Wiebe, W. J. (1998). Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A 95, 6578-6583.
139. Wuchter, C., Abbas, B., Coolen, M. J. L., Herfort, L., van Bleijswijk, J., Timmers, P., Strous, M., Teira, E., Herndl, G. J. & other authors (2006). Archaeal nitrification in the ocean. Proc Natl Acad Sci U S A 103, 12317-12322.
140. Xia, W. W., Zhang, C. X., Zeng, X. W., Feng, Y. Z., Weng, J. H., Lin, X. G., Zhu, J. G., Xiong, Z. Q., Xu, J. & other authors (2011). Autotrophic growth of nitrifying community in an agricultural soil. ISME J 5, 1226-1236.
141. Yan, J., Haaijer, S. C., Op den Camp, H. J., van Niftrik, L., Stahl, D. A., Könneke, M., Rush, D., Sinninghe Damsté, J. S., Hu, Y. Y. & Jetten, M. S. (2012). Mimicking the oxygen minimum zones: stimulating interaction of aerobic archaeal and anaerobic bacterial ammonia oxidizers in a laboratory-scale model system. Environ Microbiol 14, 3146-3158.
142. Zhalnina, K., de Quadros, P. D., Camargo, F. A. & Triplett, E. W. (2012). Drivers of archaeal ammonia-oxidizing communities in soil. Front Microbiol 3, 210.
143. Zhang, C. L., Ye, Q., Huang, Z. Y., Li, W. J., Chen, J. Q., Song, Z. Q., Zhao, W. D., Bagwell, C., Inskeep, W. P. & other authors (2008). Global occurrence of archaealamoAgenes in terrestrial hot springs. Appl Environ Microbiol 74, 6417-6426.