Complete nitrification by Nitrospira bacteria

Nature

Volumn 528, Issue 7583, 2015, Pages 504-509

  Daims, Holger ^a   Lebedeva, Elena V ^b   Pjevac, Petra ^a   Han, Ping ^a   Herbold, Craig ^a   Albertsen, Mads ^c   Jehmlich, Nico ^d   Palatinszky, Marton ^a   Vierheilig, Julia ^a   Bulaev, Alexandr ^b   Kirkegaard, Rasmus H ^c   Von Bergen, Martin ^d   Rattei, Thomas ^a   Bendinger, Bernd ^e   Nielsen, Per H ^c   Wagner, Michael ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b WINOGRADSKY INSTITUTE OF MICROBIOLOGY   (Russian Federation)

^c AALBORG UNIVERSITY   (Denmark)

^d HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^e HAMBURG UNIVERSITY OF TECHNOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; NITRATE; NITRITE; OXIDOREDUCTASE; UNSPECIFIC MONOOXYGENASE; AMMONIA MONOOXYGENASE; HYDROXYLAMINE DEHYDROGENASE; NITRIC ACID DERIVATIVE;

AGRICULTURAL SOIL; CHEMOAUTOTROPHY; CULTIVATION; GENE EXPRESSION; GROWTH RATE; MICROBIAL COMMUNITY; MICROBIOLOGY; NITRIFICATION; NITRIFYING BACTERIUM; OXIDATION; PHYLOGENETICS; SOIL MICROORGANISM; SPATIAL DISTRIBUTION;

ARTICLE; BACTERIAL GENOME; BACTERIUM CULTURE; MICROBIAL COMMUNITY; NITRIFICATION; NITRIFYING BACTERIUM; NITRITE OXIDIZER; NITROSPIRA; NONHUMAN; OXIDATION; PRIORITY JOURNAL; BACTERIUM; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHYLOGENY;

BACTERIA (MICROORGANISMS); NITROSPIRA;

AMMONIA; BACTERIA; EVOLUTION, MOLECULAR; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; NITRATES; NITRIFICATION; NITRITES; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHYLOGENY;

EID: 84951335346     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature16461     Document Type: Article

References (92)

1. Bock, E. & Wagner, M. in The Prokaryotes: A Handbook on the Biology of Bacteria (eds Dworkin, M. et al.) 457-495 (Springer, 2001).
2. Könneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543-546 (2005).
3. Winogradsky, S. Contributions a la morphologie des organismes de la nitrification. Arch. Sci. Biol. (St. Petersb.) 1, 87-137 (1892).
4. Arp, D. & Bottomley, P. J. Nitrifiers: more than 100 years from isolation to genome sequences. Microbe 1, 229-234 (2006).
5. Pfeiffer, T. & Bonhoeffer, S. Evolution of cross-feeding in microbial populations. Am. Nat. 163, E126-E135 (2004).
6. Heinrich, R. & Schuster, S. The regulation of cellular systems. (Chapman & Hall, 1996).
7. Costa, E., Pérez, J. & Kreft, J. U. Why is metabolic labour divided in nitrification? Trends Microbiol. 14, 213-219 (2006).
8. Pester, M. et al. NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ. Microbiol. 16, 3055-3071 (2014).
9. Hovanec, T. A., Taylor, L. T., Blakis, A. & Delong, E. F. Nitrospira-like bacteria associated with nitrite oxidation in freshwater aquaria. Appl. Environ. Microbiol. 64, 258-264 (1998).
10. Daims, H., Nielsen, J. L., Nielsen, P. H., Schleifer, K. H. & Wagner, M. In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Appl. Environ. Microbiol. 67, 5273-5284 (2001).
11. Watson, S. W., Bock, E., Valois, F. W., Waterbury, J. B. & Schlosser, U. Nitrospira marina gen. nov. sp. nov.: a chemolithotrophic nitrite-oxidizing bacterium. Arch. Microbiol. 144, 1-7 (1986).
12. Taylor, M. W., Radax, R., Steger, D. & Wagner, M. Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol. Mol. Biol. Rev. 71, 295-347 (2007).
13. Lebedeva, E. V. et al. Isolation and characterization of a moderately thermophilic nitrite-oxidizing bacterium from a geothermal spring. FEMS Microbiol. Ecol. 75, 195-204 (2011).
14. Martiny, A. C., Albrechtsen, H. J., Arvin, E. & Molin, S. Identification of bacteria in biofilm and bulk water samples from a nonchlorinated model drinking water distribution system: detection of a large nitrite-oxidizing population associated with Nitrospira spp. Appl. Environ. Microbiol. 71, 8611-8617 (2005).
15. Ehrich, S., Behrens, D., Lebedeva, E., Ludwig, W. & Bock, E. A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch. Microbiol. 164, 16-23 (1995).
16. Schramm, A., De Beer, D., Wagner, M. & Amann, R. Identification and activities in situ of Nitrosospira and Nitrospira spp. as dominant populations in a nitrifying fluidized bed reactor. Appl. Environ. Microbiol. 64, 3480-3485 (1998).
17. Lücker, S. et al. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc. Natl Acad. Sci. USA 107, 13479-13484 (2010).
18. Gruber-Dorninger, C. et al. Functionally relevant diversity of closely related Nitrospira in activated sludge. ISME J. 9, 643-655 (2015).
19. Koch, H. et al. Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc. Natl Acad. Sci. USA 112, 11371-11376 (2015).
20. Palatinszky, M. et al. Cyanate as an energy source for nitrifiers. Nature 524, 105-108 (2015).
21. Koch, H. et al. Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science 345, 1052-1054 (2014).
22. Mobarry, B. K., Wagner, M., Urbain, V., Rittmann, B. E. & Stahl, D. A. Phylogenetic probes for analyzing abundance and spatial organization of nitrifying bacteria. Appl. Environ. Microbiol. 62, 2156-2162 (1996).
23. Albertsen, M. et al. Genome sequences of rare, uncultured bacteria obtained by differential coverage binning of multiple metagenomes. Nature Biotechnol. 31, 533-538 (2013).
24. Arp, D. J., Chain, P. S. G. & Klotz, M. G. The impact of genome analyses on our understanding of ammonia-oxidizing bacteria. Annu. Rev. Microbiol. 61, 503-528 (2007).
25. Berube, P. M. & Stahl, D. A. The divergent AmoC3 subunit of ammonia monooxygenase functions as part of a stress response system in Nitrosomonas europaea. J. Bacteriol. 194, 3448-3456 (2012).
26. Klotz, M. G. et al. Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ. Microbiol. 10, 3150-3163 (2008).
27. Bergmann, D. J., Hooper, A. B. & Klotz, M. G. Structure and sequence conservation of hao cluster genes of autotrophic ammonia-oxidizing bacteria: evidence for their evolutionary history. Appl. Environ. Microbiol. 71, 5371-5382 (2005).
28. Klotz, M. G. & Stein, L. Y. Nitrifier genomics and evolution of the nitrogen cycle. FEMS Microbiol. Lett. 278, 146-156 (2008).
29. Rittmann, B. E., Regan, J. M. & Stahl, D. A. Nitrification as a source of soluble organic substrate in biological treatment. Water Sci. Technol. 30, 1-8 (1994).
30. Nowka, B., Off, S., Daims, H. & Spieck, E. Improved isolation strategies allowed the phenotypic differentiation of two Nitrospira strains from widespread phylogenetic lineages. FEMS Microbiol. Ecol. 91, fiu031 (2015).
31. Ushiki, N., Fujitani, H., Aoi, Y. & Tsuneda, S. Isolation of Nitrospira belonging to sublineage II from a wastewater treatment plant. Microbes Environ. 28, 346-353 (2013).
32. van Kessel, M. A. H. J. et al. Complete nitrification by a single microorganism. Nature http://dx.doi.org/10.1038/nature16459 (2015).
33. Pester, M. et al. 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 (2012).
34. Purkhold, U. et al. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl. Environ. Microbiol. 66, 5368-5382 (2000).
35. Wrighton, K. C. et al. Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337, 1661-1665 (2012).
36. Stein, L. Y. et al. Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: implications for niche adaptation. Environ. Microbiol. 9, 2993-3007 (2007).
37. Chain, P. et al. Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J. Bacteriol. 185, 2759-2773 (2003).
38. Suwa, Y. et al. Genome sequence of Nitrosomonas sp. strain AL212, an ammonia-oxidizing bacterium sensitive to high levels of ammonia. J. Bacteriol. 193, 5047-5048 (2011).
39. Norton, J. M. et al. Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl. Environ. Microbiol. 74, 3559-3572 (2008).
40. Klotz, M. G. et al. Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl. Environ. Microbiol. 72, 6299-6315 (2006).
41. Radajewski, S. et al. Identification of active methylotroph populations in an acidic forest soil by stable-isotope probing. Microbiology 148, 2331-2342 (2002).
42. Stoecker, K. et al. Cohn's Crenothrix is a filamentous methane oxidizer with an unusual methane monooxygenase. Proc. Natl Acad. Sci. USA 103, 2363-2367 (2006).
43. Schramm, A., de Beer, D., van den Heuvel, J. C., Ottengraf, S. & Amann, R. Microscale distribution of populations and activities of Nitrosospira and Nitrospira spp. along a macroscale gradient in a nitrifying bioreactor: quantification by in situ hybridization and the use of microsensors. Appl. Environ. Microbiol. 65, 3690-3696 (1999).
44. Altmann, D., Stief, P., Amann, R., De Beer, D. & Schramm, A. In situ distribution and activity of nitrifying bacteria in freshwater sediment. Environ. Microbiol. 5, 798-803 (2003).
45. Foesel, B. U. et al. Nitrosomonas Nm143-like ammonia oxidizers and Nitrospira marina-like nitrite oxidizers dominate the nitrifier community in a marine aquaculture biofilm. FEMS Microbiol. Ecol. 63, 192-204 (2008).
46. Winkler, M. K. H., Bassin, J. P., Kleerebezem, R., Sorokin, D. Y. & van Loosdrecht, M. C. M. Unravelling the reasons for disproportion in the ratio of AOB and NOB in aerobic granular sludge. Appl. Microbiol. Biotechnol. 94, 1657-1666 (2012).
47. Maixner, F. et al. Nitrite concentration influences the population structure of Nitrospira-like bacteria. Environ. Microbiol. 8, 1487-1495 (2006).
48. Nowka, B., Daims, H. & Spieck, E. Comparison of oxidation kinetics of nitrite-oxidizing bacteria: nitrite availability as a key factor in niche differentiation. Appl. Environ. Microbiol. 81, 745-753 (2015).
49. Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R. & Stahl, D. A. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461, 976-979 (2009).
50. Prosser, J. I. & Nicol, G. W. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 20, 523-531 (2012).
51. Lebedeva, E. V. et al. Enrichment and genome sequence of the group I.1a ammonia-oxidizing Archaeon "Ca. Nitrosotenuis uzonensis" representing a clade globally distributed in thermal habitats. PLoS One 8, e80835 (2013).
52. Widdel, F. Anaerober Abbau von Fettsäuren und Benzoesäure durch neu isolierte Arten Sulfat-reduzierender Bakterien. PhD thesis, Univ. Göttingen (1980).
53. Kandeler, E. & Gerber, H. Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol. Fertil. Soils 6, 68-72 (1988).
54. Hood-Nowotny, R., Hinko-Najera Umana, N., Inselbacher, E., Oswald-Lachouani, P. & Wanek, W. Alternative methods for measuring inorganic, organic, and total dissolved nitrogen in soil. Soil Sci. Soc. Am. J. 74, 1018-1027 (2010).
55. Griess-Romijn van Eck, E. Physiological and chemical tests for drinking water. NEN 1056 IV-2 Nederlands Normalisatie Instituut, Rijswijk, The Netherlands (1966).
56. Miranda, K. M., Espey, M. G. & Wink, D. A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 5, 62-71 (2001).
57. Daims, H., Stoecker, K. & Wagner, M. in Molecular Microbial Ecology (eds Osborn, A. M. & Smith, C. J.) 213-239 (Bios-Garland, 2005).
58. Daims, H., Brühl, A., Amann, R., Schleifer, K.-H. & Wagner, M. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Syst. Appl. Microbiol. 22, 434-444 (1999).
59. Amann, R. I. et al. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56, 1919-1925 (1990).
60. Daims, H. Use of fluorescence in situ hybridization and the daime image analysis program for the cultivation-independent quantification of microorganisms in environmental and medical samples. Cold Spring Harb. Protoc. 2009, t5253 (2009).
61. Daims, H., Lücker, S. & Wagner, M. daime, a novel image analysis program for microbial ecology and biofilm research. Environ. Microbiol. 8, 200-213 (2006).
62. Sorokin, D. Y. et al. Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J. 6, 2245-2256 (2012).
63. Rotthauwe, J.-H., Witzel, K.-P. & Liesack, W. The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl. Environ. Microbiol. 63, 4704-4712 (1997).
64. Tourna, M., Freitag, T. E., Nicol, G. W. & Prosser, J. I. Growth, activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ. Microbiol. 10, 1357-1364 (2008).
65. Ochsenreiter, T., Selezi, D., Quaiser, A., Bonch-Osmolovskaya, L. & Schleper, C. Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ. Microbiol. 5, 787-797 (2003).
66. Angel, R., Claus, P. & Conrad, R. Methanogenic archaea are globally ubiquitous in aerated soils and become active under wet anoxic conditions. ISME J. 6, 847-862 (2012).
67. Angel, R. Total nucleic acid extraction from soil. Protoc. Exch. http://dx.doi.org/10.1038/protex.2012.046 (2012).
68. Watson, M. et al. poRe: an R package for the visualization and analysis of nanopore sequencing data. Bioinformatics 31, 114-115 (2015).
69. Hackl, T., Hedrich, R., Schultz, J. & Förster, F. proovread: large-scale high-accuracy PacBio correction through iterative short read consensus. Bioinformatics 30, 3004-3011 (2014).
70. Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).
71. Dupont, C. L. et al. Genomic insights to SAR86, an abundant and uncultivated marine bacterial lineage. ISME J. 6, 1186-1199 (2012).
72. Huson, D. H., Mitra, S., Ruscheweyh, H. J., Weber, N. & Schuster, S. C. Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21, 1552-1560 (2011).
73. Gregor, I., Dröge, J., Schirmer, M., Quince, C. & McHardy, A. C. PhyloPythiaS+: A self-training method for the rapid reconstruction of low-ranking taxonomic bins from metagenomes. Preprint at http://arxiv.org/abs/1406.7123 (2014).
74. Dick, G. J. et al. Community-wide analysis of microbial genome sequence signatures. Genome Biol. 10, R85 (2009).
75. Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477 (2012).
76. Boetzer, M. & Pirovano, W. SSPACE-LongRead: scaffolding bacterial draft genomes using long read sequence information. BMC Bioinformatics 15, 211 (2014).
77. Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072-1075 (2013).
78. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043-1055 (2015).
79. Vallenet, D. et al. MicroScope - an integrated microbial resource for the curation and comparative analysis of genomic and metabolic data. Nucleic Acids Res. 41, D636-D647 (2013).
80. Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312-1313 (2014).
81. Finn, R. D. et al. Pfam: the protein families database. Nucleic Acids Res. 42, D222-D230 (2014).
82. Benson, D. A. et al. GenBank. Nucleic Acids Res. 43, D30-D35 (2015).
83. Markowitz, V. M. et al. IMG 4 version of the integrated microbial genomes comparative analysis system. Nucleic Acids Res. 42, D560-D567 (2014).
84. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
85. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460-2461 (2010).
86. Katoh, K., Misawa, K., Kuma, K. & Miyata, T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30, 3059-3066 (2002).
87. Lartillot, N., Lepage, T. & Blanquart, S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286-2288 (2009).
88. Edgar, R. C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792-1797 (2004).
89. Ludwig, W. et al. ARB: a software environment for sequence data. Nucleic Acids Res. 32, 1363-1371 (2004).
90. Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539-542 (2012).
91. Richter, M. & Rosselló-Móra, R. Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl Acad. Sci. USA 106, 19126-19131 (2009).
92. The R Project. R: A language and environment for statistical computing. https://www.r-project.org/ (R Foundation for Statistical Computing, 2013).