Homologues of nitrite reductases in ammonia-oxidizing archaea: Diversity and genomic context

Environmental Microbiology

Volumn 12, Issue 4, 2010, Pages 1075-1088

  Bartossek, Rita ^a,b   Nicol, Graeme W ^c   Lanzen, Anders ^a   Klenk, Hans Peter ^d   Schleper, Christa ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF ABERDEEN   (United Kingdom)

^d LEIBNIZ INSTITUTE DSMZ GERMAN COLLECTION OF MICROORGANISMS AND CELL CULTURES   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEA; BACTERIA (MICROORGANISMS); CANDIDATUS NITROSOPUMILUS MARITIMUS; CENARCHAEUM SYMBIOSUM;

AMMONIA; ARCHAEAL DNA; NITRITE REDUCTASE; NITRITE REDUCTASE, COPPER CONTAINING; NITRITE REDUCTASE, COPPER-CONTAINING; OXIDOREDUCTASE;

AMINO ACID SEQUENCE; ARCHAEAL GENOME; ARCHAEBACTERIUM; ARTICLE; BACTERIUM; CLASSIFICATION; DNA SEQUENCE; ENZYMOLOGY; GENE LIBRARY; GENETICS; METABOLISM; METAGENOMICS; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; AMMONIA; ARCHAEA; BACTERIA; DNA, ARCHAEAL; GENOME, ARCHAEAL; GENOMIC LIBRARY; METAGENOMICS; MOLECULAR SEQUENCE DATA; NITRITE REDUCTASES; OXIDATION-REDUCTION; OXIDOREDUCTASES; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

EID: 77954639120     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02153.x     Document Type: Article

References (69)

1. Beaumont HJ, Hommes NG, Sayavedra-Soto LA, Arp DJ, Arciero DM, Hooper AB. Nitrite reductase of Nitrosomonas europaea is not essential for production of gaseous nitrogen oxides and confers tolerance to nitrite. J Bacteriol 2002, 184:2557-2560.
2. Bell SD, Kosa PL, Sigler PB, Jackson SP. Orientation of the transcription preinitiation complex in archaea. Proc Natl Acad Sci USA 1999, 96:13662-13667.
3. Beman JM, Roberts KJ, Wegley L, Rohwer F, Francis CA. Distribution and diversity of archaeal ammonia monooxygenase genes associated with corals. Appl Environ Microbiol 2007, 73:5642-5647.
4. Braker G, Zhou J, Wu L, Devol AH, Tiedje JM. Nitrite reductase genes (nirK and nirS) as functional markers to investigate diversity of denitrifying bacteria in pacific northwest marine sediment communities. Appl Environ Microbiol 2000, 66:2096-2104.
5. Brochier-Armanet C, Gribaldo S, Forterre P. A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya. Biol Direct 2008a, 3:54.
6. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 2008b, 6:245-252.
7. Cabello P, Roldan MD, Moreno-Vivian C. Nitrate reduction and the nitrogen cycle in archaea. Microbiology 2004, 150:3527-3546.
8. Cantera JJ, Stein LY. Molecular diversity of nitrite reductase genes (nirK) in nitrifying bacteria. Environ Microbiol 2007a, 9:765-776.
9. Cantera JJ, Stein LY. Role of nitrite reductase in the ammonia-oxidizing pathway of Nitrosomonas europaea. Arch Microbiol 2007b, 188:349-354.
10. Canters GW, Kolczak U, Armstrong F, Jeuken LJ, Camba R, Sola M. The effect of pH and ligand exchange on the redox properties of blue copper proteins. Faraday Discuss 2000, 116:257-268. discussion
11. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics 2007, 23:673-679.
12. Dodd FE, Hasnain SS, Abraham ZH, Eady RR, Smith BE. Structures of a blue-copper nitrite reductase and its substrate-bound complex. Acta Crystallogr D Biol Crystallogr 1997, 53:406-418.
13. Dore JE, Popp BN, Karl DM, Sansone FJ. A large source of atmospheric nitrous oxide from subtropical North Pacific surface waters. Nature 1998, 396:63-66.
14. Ellis MJ, Grossmann JG, Eady RR, Hasnain SS. Genomic analysis reveals widespread occurrence of new classes of copper nitrite reductases. J Biol Inorg Chem 2007, 12:1119-1127.
15. Ewing B, Hillier L, Wendl MC, Green P. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 1998, 8:175-185.
16. Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 2005, 102:14683-14688.
17. Garcia-Ruiz R, Baggs EM. N2O emission from soil following combined application of fertiliser-N and ground weed residues. Plant Soil 2007, 299:263-274.
18. Giri AV, Anishetty S, Gautam P. Functionally specified protein signatures distinctive for each of the different blue copper proteins. BMC Bioinformatics 2004, 5:127.
19. Godden JW, Turley S, Teller DC, Adman ET, Liu MY, Payne WJ, LeGall J. The 2.3 angstrom X-ray structure of nitrite reductase from Achromobacter cycloclastes. Science 1991, 253:438-442.
20. Gordon D, Abajian C, Green P. Consed: a graphical tool for sequence finishing. Genome Res 1998, 8:195-202.
21. Goreau TJ, Kaplan WA, Wofsy SC, McElroy MB, Valois FW, Watson SW. Production of NO2- and N2O by nitrifying bacteria at reduced concentrations of oxygen. Appl Environ Microbiol 1980, 40:526-532.
22. Griffiths RI, Whiteley AS, O'Donnell AG, Bailey MJ. Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 2000, 66:5488-5491.
23. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
24. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 1999, 41:95-98.
25. Hallam SJ, Konstantinidis KT, Putnam N, Schleper C, Watanabe Y, Sugahara J. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc Natl Acad Sci USA 2006a, 103:18296-18301.
26. Hallam SJ, Mincer TJ, Schleper C, Preston CM, Roberts K, Richardson PM, DeLong EF. Pathways of carbon assimilation and ammonia oxidation suggested by environmental genomic analyses of marine Crenarchaeota. PLoS Biol 2006b, 4:e95.
27. Hallin S, Lindgren PE. PCR detection of genes encoding nitrite reductase in denitrifying bacteria. Appl Environ Microbiol 1999, 65:1652-1657.
28. Hatzenpichler R, Lebedeva EV, Spieck E, Stoecker K, Richter A, Daims H, Wagner M. A moderately thermophilic ammonia-oxidizing crenarchaeote from a hot spring. Proc Natl Acad Sci USA 2008, 105:2134-2139.
29. He J, Shen J, Zhang L, Zhu Y, Zheng Y, Xu M, Di HJ. 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 2007, 9:2364-2374.
30. Heylen K, Gevers D, Vanparys B, Wittebolle L, Geets J, Boon N, De Vos P. The incidence of nirS and nirK and their genetic heterogeneity in cultivated denitrifiers. Environ Microbiol 2006, 8:2012-2021.
31. Jones CM, Stres B, Rosenquist M, Hallin S. Phylogenetic analysis of nitrite, nitric oxide, and nitrous oxide respiratory enzymes reveal a complex evolutionary history for denitrification. Mol Biol Evol 2008, 25:1955-1966.
32. Könneke M, Bernhard AE, Torre JR, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 2005, 437:543-546.
33. Kowalchuk GA, Stephen JR. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 2001, 55:485-529.
34. Kukimoto M, Nishiyama M, Murphy ME, Turley S, Adman ET, Horinouchi S, Beppu T. X-ray structure and site-directed mutagenesis of a nitrite reductase from Alcaligenes faecalis S-6: roles of two copper atoms in nitrite reduction. Biochemistry 1994, 33:5246-5252.
35. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 2006, 442:806-809.
36. Lipschultz F, Zafiriou OC, Wofsy SC. Production of NO and N2O by soil nitrifying bacteria. Nature 1981, 294:641-643.
37. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997, 25:955-964.
38. MacPherson IS, Murphy ME. Type-2 copper-containing enzymes. Cell Mol Life Sci 2007, 64:2887-2899.
39. Markowitz VM, Ivanova NN, Szeto E, Palaniappan K, Chu K, Dalevi D. IMG/M: a data management and analysis system for metagenomes. Nucleic Acids Res 2008, 36:D534-D538.
40. Martin-Cuadrado AB, Lopez-Garcia P, Alba JC, Moreira D, Monticelli L, Strittmatter A. Metagenomics of the deep Mediterranean, a warm bathypelagic habitat. PLoS ONE 2007, 2:e914.
41. Nicol GW, Leininger S, Schleper C, Prosser JI. The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 2008, 10:2966-2978.
42. Nojiri M, Xie Y, Inoue T, Yamamoto T, Matsumura H, Kataoka K. Structure and function of a hexameric copper-containing nitrite reductase. Proc Natl Acad Sci USA 2007, 104:4315-4320.
43. Norton JM, Klotz MG, Stein LY, Arp DJ, Bottomley PJ, Chain PS. Complete genome sequence of Nitrosospira multiformis, an ammonia-oxidizing bacterium from the soil environment. Appl Environ Microbiol 2008, 74:3559-3572.
44. 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 2003, 5:787-797.
45. Philippot L. Denitrifying genes in bacterial and Archaeal genomes. Biochim Biophys Acta 2002, 1577:355-376.
46. Prieme A, Braker G, Tiedje JM. Diversity of nitrite reductase (nirK and nirS) gene fragments in forested upland and wetland soils. Appl Environ Microbiol 2002, 68:1893-1900.
47. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M. 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 2000, 66:5368-5382.
48. Quaiser A, Ochsenreiter T, Klenk HP, Kletzin A, Treusch AH, Meurer G. First insight into the genome of an uncultivated crenarchaeote from soil. Environ Microbiol 2002, 4:603-611.
49. Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, Lopez R. InterProScan: protein domains identifier. Nucleic Acids Res 2005, 33:W116-W120.
50. Reigstad LJ, Richter A, Daims H, Urich T, Schwark L, Schleper C. Nitrification in terrestrial hot springs of Iceland and Kamchatka. FEMS Microbiol Ecol 2008, 64:167-174.
51. Ritchie GA, Nicholas DJ. The partial characterization of purified nitrite reductase and hydroxylamine oxidase from Nitrosomonas europaea. Biochem J 1974, 138:471-480.
52. Sakurai T, Kataoka K. Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem Rec 2007, 7:220-229.
53. Schleper C, Jurgens G, Jonuscheit M. Genomic studies of uncultivated archaea. Nat Rev Microbiol 2005, 3:479-488.
54. Schmidt I. Chemoorganoheterotrophic growth of Nitrosomonas europaea and Nitrosomonas eutropha. Curr Microbiol 2009, 59:130-138.
55. Schmidt I, van Spanning RJ, Jetten MS. Denitrification and ammonia oxidation by Nitrosomonas europaea wild-type, and NirK- and NorB-deficient mutants. Microbiology 2004, 150:4107-4114.
56. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: molecular evolutionary genetics analysis (mega) software version 4.0. Mol Biol Evol 2007, 24:1596-1599.
57. Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS. The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 2001, 29:22-28.
58. Tobari J, Harada Y. Amicyanin: an electron acceptor of methylamine dehydrogenase. Biochem Biophys Res Commun 1981, 101:502-508.
59. Torarinsson E, Klenk HP, Garrett RA. Divergent transcriptional and translational signals in Archaea. Environ Microbiol 2005, 7:47-54.
60. de la Torre JR, Walker CB, Ingalls AE, Konneke M, Stahl DA. Cultivation of a thermophilic ammonia oxidizing archaeon synthesizing crenarchaeol. Environ Microbiol 2008, 10:810-818.
61. Treusch AH, Kletzin A, Raddatz G, Ochsenreiter T, Quaiser A, Meurer G. Characterization of large-insert DNA libraries from soil for environmental genomic studies of Archaea. Environ Microbiol 2004, 6:970-980.
62. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol 2005, 7:1985-1995.
63. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA. Environmental genome shotgun sequencing of the Sargasso Sea. Science 2004, 304:66-74.
64. Webster EA, Hopkins DW. Nitrogen and oxygen isotope ratios of nitrous oxide emitted from soil and produced by nitrifying and denitrifying bacteria. Biol Fertil Soils 1996, 22:326-330.
65. Wuchter C, Abbas B, Coolen MJL, Herfort L, van Bleijswijk J, Timmers P. Archaeal nitrification in the ocean. Proc Natl Acad Sci USA 2006, 103:12317-12322.
66. Yamaguchi K, Kobayashi M, Kataoka K, Suzuki S. Characterization of two Cu-containing protein fragments obtained by limited proteolysis of Hyphomicrobium denitrificans A3151 nitrite reductase. Biochem Biophys Res Commun 2003, 300:36-40.
67. Yamaguchi K, Kataoka K, Kobayashi M, Itoh K, Fukui A, Suzuki S. Characterization of two type 1 Cu sites of Hyphomicrobium denitrificans nitrite reductase: a new class of copper-containing nitrite reductases. Biochemistry 2004, 43:14180-14188.
68. Yoshida N, Morimoto H, Hirano M, Koike I, Matsuo S, Wada E. Nitrification rates and 15N abundances of N2O and NO3- in the western North Pacific. Nature 1989, 342:895-897.
69. Zumft WG. Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 1997, 61:533-616.