1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 64, Issue Pt_8

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

Abstract

A mesophilic, neutrophilic and aerobic, ammonia-oxidizing archaeon, strain EN76, was isolated from garden soil in Vienna (Austria). Cells were irregular cocci with a diameter of 0.6–0.9 µm and possessed archaella and archaeal pili as cell appendages. Electron microscopy also indicated clearly discernible areas of high and low electron density, as well as tubule-like structures. Strain EN76 had an S-layer with p3 symmetry, so far only reported for members of the . Crenarchaeol was the major core lipid. The organism gained energy by oxidizing ammonia to nitrite aerobically, thereby fixing CO, but growth depended on the addition of small amounts of organic acids. The optimal growth temperature was 42 °C and the optimal pH was 7.5, with ammonium and pyruvate concentrations of 2.6 and 1 mM, respectively. The genome of strain EN76 had a DNA G+C content of 52.7 mol%. Phylogenetic analyses of 16S rRNA genes showed that strain EN76 is affiliated with the recently proposed phylum , sharing 85 % 16S rRNA gene sequence identity with the closest cultivated relative ‘ Nitrosopumilus maritimus’ SCM1, a marine ammonia-oxidizing archaeon, and a maximum of 81 % 16S rRNA gene sequence identity with members of the phyla and and any of the other recently proposed phyla (e.g. ‘’ and ‘’). We propose the name gen. nov., sp. nov. to accommodate strain EN76. The type strain of is strain EN76 ( = DSM 26422 = JMC 19564) Additionally, we propose the family fam. nov., the order ord. nov. and the class classis nov.

  • Published Online:
Funding
This study was supported by the:
  • FWF (Austrian Science Fund) (Award P25369 and P23000)
  • Krajete GmbH
© 2014 IUMS
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijs.0.063172-0
2014-08-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/64/8/2738.html?itemId=/content/journal/ijsem/10.1099/ijs.0.063172-0&mimeType=html&fmt=ahah

References

  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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 ammonia-oxidizing archaea. . ISME J 7, 1620–1631. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  5. Andrews S. C., Robinson A. K., Rodríguez-Quiñones F. ( 2003 ). Bacterial iron homeostasis. . FEMS Microbiol Rev 27, 215–237. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  8. Baumeister W., Lembcke G. ( 1992 ). Structural features of archaebacterial cell envelopes. . J Bioenerg Biomembr 24, 567–575. [View Article] [PubMed]
    [Google Scholar]
  9. Berg I. A., Kockelkorn D., Buckel W., Fuchs G. ( 2007 ). A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in archaea. . Science 318, 1782–1786. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  11. Box G. E. P., Draper N. R. ( 1987 ). Empirical Model-Building and Response Surfaces. Oxford:: Wiley;.
     [Google Scholar]
  12. Box G. E. P., Lucas H. L. ( 1959 ). Design of experiments in non-linear situations. . Biometrika 46, 77–90. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  17. Deatherage J. F., Taylor K. A., Amos L. A. ( 1983 ). Three-dimensional arrangement of the cell wall protein of Sulfolobus acidocaldarius . . J Mol Biol 167, 823–848. [View Article] [PubMed]
    [Google Scholar]
  18. DeLong E. F. ( 1992 ). Archaea in coastal marine environments. . Proc Natl Acad Sci U S A 89, 5685–5689. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  20. Derringer G., Suich R. ( 1980 ). Simultaneous optimization of several response variables. . J Qual Technol 12, 214–219.
     [Google Scholar]
  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. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  23. Dridi B., Fardeau M.-L., Ollivier B., Raoult D., Drancourt M. ( 2012 ). Methanomassiliicoccus luminyensis gen. nov., sp. nov., a methanogenic archaeon isolated from human faeces. . Int J Syst Evol Microbiol 62, 1902–1907. [View Article] [PubMed]
    [Google Scholar]
  24. Durbin A. M., Teske A. ( 2010 ). Sediment-associated microdiversity within the marine group I Crenarchaeota. . Environ Microbiol Rep 2, 693–703. [View Article] [PubMed]
    [Google Scholar]
  25. Edgar R. C. ( 2004 ). muscle: multiple sequence alignment with high accuracy and high throughput. . Nucleic Acids Res 32, 1792–1797. [View Article] [PubMed]
    [Google Scholar]
  26. Eichler J. ( 2003 ). Facing extremes: archaeal surface-layer (glyco)proteins. . Microbiology 149, 3347–3351. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  32. Fernandez-Castillo R., Rodriguez-Valera F., Gonzalez-Ramos J., Ruiz-Berraquero F. ( 1986 ). Accumulation of poly(β-hydroxybutyrate) by halobacteria. . Appl Environ Microbiol 51, 214–216.[PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  35. Fuhrman J. A., McCallum K., Davis A. A. ( 1992 ). Novel major archaebacterial group from marine plankton. . Nature 356, 148–149. [View Article] [PubMed]
    [Google Scholar]
  36. Gordon D. A., Giovannoni S. J. ( 1996 ). Detection of stratified microbial populations related to Chlorobium and Fibrobacter species in the Atlantic and Pacific oceans. . Appl Environ Microbiol 62, 1171–1177.[PubMed]
    [Google Scholar]
  37. Grogan D. W. ( 1996 ). Organization and interactions of cell envelope proteins of the extreme thermoacidophile Sulfolobus acidocaldarius . . Can J Microbiol 42, 1163–1171. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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 crenarchaeote Cenarchaeum symbiosum . . Proc Natl Acad Sci U S A 103, 18296–18301. [View Article] [PubMed]
    [Google Scholar]
  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 marine Crenarchaeota . . PLoS Biol 4, e95. [View Article] [PubMed]
    [Google Scholar]
  42. Hatzenpichler R. ( 2012 ). Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. . Appl Environ Microbiol 78, 7501–7510. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  45. Hershberger K. L., Barns S. M., Reysenbach A. L., Dawson S. C., Pace N. R. ( 1996 ). Wide diversity of Crenarchaeota. . Nature 384, 420. [View Article] [PubMed]
    [Google Scholar]
  46. Hooper A. B., Terry K. R. ( 1979 ). Hydroxylamine oxidoreductase of Nitrosomonas. Production of nitric oxide from hydroxylamine. . Biochim Biophys Acta 571, 12–20. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  48. Huber H., Burggraf S., Mayer T., Wyschkony I., Rachel R., Stetter K. O. ( 2000 ). Ignicoccus gen. nov., a novel genus of hyperthermophilic, chemolithoautotrophic Archaea, represented by two new species, Ignicoccus islandicus sp. nov. and Ignicoccus pacificus sp. nov.. Int J Syst Evol Microbiol 50, 2093–2100. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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.[PubMed]
    [Google Scholar]
  51. Jarrell K. F., Albers S.-V. ( 2012 ). The archaellum: an old motility structure with a new name. . Trends Microbiol 20, 307–312. [View Article] [PubMed]
    [Google Scholar]
  52. Jia Z., Conrad R. ( 2009 ). Bacteria rather than Archaea dominate microbial ammonia oxidation in an agricultural soil. . Environ Microbiol 11, 1658–1671. [View Article] [PubMed]
    [Google Scholar]
  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 Mid-Ocean Ridge. . Proc Natl Acad Sci U S A 109, E2846–E2855. [View Article] [PubMed]
    [Google Scholar]
  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 ammonia-oxidizing archaeon of mesophilic crenarchaeal group I.1a from an agricultural soil. . Appl Environ Microbiol 77, 8635–8647. [View Article] [PubMed]
    [Google Scholar]
  55. Jurgens G., Lindström K., Saano A. ( 1997 ). Novel group within the kingdom Crenarchaeota from boreal forest soil. . Appl Environ Microbiol 63, 803–805.[PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  58. Katoh K., Toh H. ( 2010 ). Parallelization of the mafft multiple sequence alignment program. . Bioinformatics 26, 1899–1900. [View Article] [PubMed]
    [Google Scholar]
  59. Katoh K., Kuma K., Toh H., Miyata T. ( 2005 ). mafft version 5: improvement in accuracy of multiple sequence alignment. . Nucleic Acids Res 33, 511–518. [View Article] [PubMed]
    [Google Scholar]
  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, “Candidatus Nitrosoarchaeum koreensis” MY1. . J Bacteriol 193, 5539–5540. [View Article] [PubMed]
    [Google Scholar]
  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;.
     [Google Scholar]
  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, pyrite-oxidizing Acidithiobacillus isolate HV2/2, and their possible involvement in pyrite oxidation. . Arch Microbiol 193, 867–882. [View Article] [PubMed]
    [Google Scholar]
  63. Klingl A., Flechsler J., Heimerl T., Rachel R. ( 2013 ). Archaeal cells. . In eLS. Chichester:: Wiley;. [View Article]
    [Google Scholar]
  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 Cavicchioli R. . Washington, DC:: American Society for Microbiology;. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  69. Leisch N., Dirks U., Gruber-Vodicka H. R., Schmid M., Sterrer W., Ott J. A. ( 2011 ). Microanatomy of the trophosome region of Paracatenula cf. polyhymnia (Catenulida, Platyhelminthes) and its intracellular symbionts. . Zoomorphology 130, 261–271. [View Article] [PubMed]
    [Google Scholar]
  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 re-investigated. . J Microsc 161, 263–278. [View Article]
    [Google Scholar]
  71. Lembcke G., Baumeister W., Beckmann E., Zemlin F. ( 1993 ). Cryo-electron microscopy of the surface protein of Sulfolobus shibatae . . Ultramicroscopy 49, 397–406. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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.[PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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;. [CrossRef]
    [Google Scholar]
  78. Mosier A. C., Allen E. E., Kim M., Ferriera S., Francis C. A. ( 2012a ). Genome sequence of “Candidatus Nitrosoarchaeum limnia” BG20, a low-salinity ammonia-oxidizing archaeon from the San Francisco Bay estuary. . J Bacteriol 194, 2119–2120. [View Article] [PubMed]
    [Google Scholar]
  79. Mosier A. C., Allen E. E., Kim M., Ferriera S., Francis C. A. ( 2012b ). Genome sequence of “Candidatus Nitrosopumilus salaria” BD31, an ammonia-oxidizing archaeon from the San Francisco Bay estuary. . J Bacteriol 194, 2121–2122. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  82. Nicol G. W., Schleper C. ( 2006 ). Ammonia-oxidising Crenarchaeota: important players in the nitrogen cycle?. Trends Microbiol 14, 207–212. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  85. Offre P., Prosser J. I., Nicol G. W. ( 2009 ). Growth of ammonia-oxidizing archaea in soil microcosms is inhibited by acetylene. . FEMS Microbiol Ecol 70, 99–108. [View Article] [PubMed]
    [Google Scholar]
  86. Park S. J., Kim J. G., Jung M. Y., Kim S. J., Cha I. T., Ghai R., Martín-Cuadrado 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. [View Article] [PubMed]
    [Google Scholar]
  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 thaumarchaeon Nitrosopumilus maritimus . . Mol Microbiol 82, 555–566. [View Article] [PubMed]
    [Google Scholar]
  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 amoA genes from soils of four different geographic regions. . Environ Microbiol 14, 525–539. [View Article] [PubMed]
    [Google Scholar]
  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 of Candidatus Nitrososphaera gargensis, a thermophilic group I.1b archaeon. . ISME J 4, 542–552. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  91. Prosser J. I., Nicol G. W. ( 2012 ). Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. . Trends Microbiol 20, 523–531. [View Article] [PubMed]
    [Google Scholar]
  92. Prüschenk R., Baumeister W. ( 1987 ). Three-dimensional structure of the surface protein of Sulfolobus solfataricus . . Eur J Cell Biol 45, 185–191.
     [Google Scholar]
  93. Prüschenk R., Baumeister W., Zillig W. ( 1987 ). Surface structure variants in different species of Sulfolobus . . FEMS Microbiol Lett 43, 327–330. [View Article]
    [Google Scholar]
  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. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  96. Rappé M. S., Giovannoni S. J. ( 2003 ). The uncultured microbial majority. . Annu Rev Microbiol 57, 369–394. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  99. Rittmann S., Herwig C. ( 2012 ). A comprehensive and quantitative review of dark fermentative biohydrogen production. . Microb Cell Fact 11, 115. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  101. Schauss K., Focks A., Leininger S., Kotzerke A., Heuer H., Thiele-Bruhn 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. [View Article] [PubMed]
    [Google Scholar]
  102. Schleper C., Nicol G. W. ( 2010 ). Ammonia-oxidising archaea – physiology, ecology and evolution. . Adv Microb Physiol 57, 1–41. [View Article] [PubMed]
    [Google Scholar]
  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.[PubMed]
    [Google Scholar]
  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.[PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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 multiformis to nitrification inhibitors. . FEMS Microbiol Lett 344, 121–129. [View Article] [PubMed]
    [Google Scholar]
  108. Shively J. M., Ball F., Brown D. H., Saunders R. E. ( 1973 ). Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus . . Science 182, 584–586. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  111. Sleytr U. B., Messner P., Pum D., Sára M. ( 1993 ). Crystalline bacterial cell surface layers. . Mol Microbiol 10, 911–916. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. . Environ Microbiol 14, 3122–3145. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  117. Stahl D. A., de la Torre J. R. ( 2012 ). Physiology and diversity of ammonia-oxidizing archaea. . Annu Rev Microbiol 66, 83–101. [View Article] [PubMed]
    [Google Scholar]
  118. Stamatakis A. ( 2006 ). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. . Bioinformatics 22, 2688–2690. [View Article] [PubMed]
    [Google Scholar]
  119. Stamatakis A., Hoover P., Rougemont J. ( 2008 ). A rapid bootstrap algorithm for the RAxML Web servers. . Syst Biol 57, 758–771. [View Article] [PubMed]
    [Google Scholar]
  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.[PubMed]
    [Google Scholar]
  121. Stieglmeier M., Alves R. J. E., Schleper C. ( 2014a ). Thaumarchaeota . . In The Prokaryotes, , 4th edn.. Edited by Rosenberg E., DeLong E. F., Lory S., Stackebrandt E., Thompson F. . Berlin & Heidelberg:: Springer; (in press).
     [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  124. Taylor K. A., Deatherage J. F., Amos L. A. ( 1982 ). Structure of the S-layer of Sulfolobus acidocaldarius . . Nature 299, 840–842. [View Article]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  127. Treusch A. H., Leininger S., Kletzin A., Schuster S. C., Klenk H. P., Schleper C. ( 2005 ). Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. . Environ Microbiol 7, 1985–1995. [View Article] [PubMed]
    [Google Scholar]
  128. Tyson G. W., Banfield J. F. ( 2005 ). Cultivating the uncultivated: a community genomics perspective. . Trends Microbiol 13, 411–415. [View Article] [PubMed]
    [Google Scholar]
  129. Urakawa H., Martens-Habbena W., Stahl D. A. ( 2011 ). Physiology and genomics of ammonia-oxidizing archaea. . In Nitrification, pp. 117–155. Edited by Ward B. B., Arp D. J., Klotz M. G. . Washington, DC:: American Society for Microbiology;.
     [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  133. van Niftrik L., Jetten M. S. M. ( 2012 ). Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. . Microbiol Mol Biol Rev 76, 585–596. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  135. Veith A., Klingl A., Zolghadr B., Lauber K., Mentele R., Lottspeich F., Rachel R., Albers S. V., Kletzin A. ( 2009 ). Acidianus, Sulfolobus and Metallosphaera surface layers: structure, composition and gene expression. . Mol Microbiol 73, 58–72. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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 maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. . Proc Natl Acad Sci U S A 107, 8818–8823. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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. [View Article] [PubMed]
    [Google Scholar]
  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 archaeal amoA genes in terrestrial hot springs. . Appl Environ Microbiol 74, 6417–6426. [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijs.0.063172-0
Loading
Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota
Int J Syst Evol Microbiol 64, 2738 (2014); https://doi.org/10.1099/ijs.0.063172-0
/content/journal/ijsem/10.1099/ijs.0.063172-0
/content/journal/ijsem/10.1099/ijs.0.063172-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error