Nitrifier genomics and evolution of the nitrogen cycle

FEMS Microbiology Letters

Volumn 278, Issue 2, 2008, Pages 146-156

  Klotz, Martin G ^a,b   Stein, Lisa Y ^c  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b University of Louisville School of Medicine   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anammox; Catabolic modules; Denitrification; Evolution; Nitrification; Nitrogen cycle

Indexed keywords

AMMONIA;

AMMONIFICATION; CHEMICAL ANALYSIS; DENITRIFICATION; GENE SEQUENCE; GENOMICS; GEOCHEMISTRY; MOLECULAR GENETICS; NITROGEN CYCLE; NONHUMAN; OCEANOGRAPHY; OXIDATION; PRIORITY JOURNAL; PROKARYOTE; SHORT SURVEY;

AMMONIA; BIOGENESIS; EVOLUTION, MOLECULAR; GENOMICS; MODELS, BIOLOGICAL; NITRATES; NITROGEN; NITROSOMONAS; PROKARYOTIC CELLS;

PROKARYOTA;

EID: 37249025200     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2007.00970.x     Document Type: Short Survey

References (92)

1. Anbar AD Knoll AH (2002) Proterozoic ocean chemistry and evolution: a bioinorganic bridge? Science 297 : 1137 1142.
2. Arciero DM, Pierce BS, Hendrich MP Hooper AB (2002) Nitrosocyanin, a red cupredoxin-like protein from Nitrosomonas europaea. Biochemistry 41 : 1703 1709.
3. Arp DJ, Chain PSG Klotz MG (2007) The impact of genome analyses on our understanding of ammonia-oxidizing bacteria. Ann Rev Microbiol 61 : 21 58.
4. Beaumont HJE, Hommes NG, Sayavedra-Soto LA, Arp DJ, Arciero DM, Hooper AB, Westerhoff HV van Spanning RJM (2002) Nitrite reductase of Nitrosomonas europaea is not essential for production of gaseous nitrogen oxides and confers tolerance to nitrite. J Bacteriol 184 : 2557 2560.
5. Beaumont HJE, Lens SI, Reijnders WNM, Westerhoff HV van Spanning RJM (2004) Expression of nitrite reductase in Nitrosomonas europaea involves NsrR, a novel nitrite-sensitive transcription repressor. Mol Microbiol 54 : 148 158.
6. Beaumont HJE, van Schooten B, Lens SI, Westerhoff HV van Spanning RJM (2004) Nitrosomonas europaea expresses a nitric oxide reductase during nitrification. J Bacteriol 186 : 4417 4421.
7. Beaumont HJE, Lens SI, Westerhoff HV van Spanning RJM (2005) Novel nirK cluster genes in Nitrosomonas europaea are required for NirK-dependent tolerance to nitrite. J Bacteriol 187 : 6849 6851.
8. Bergmann DJ, Zahn JA, Hooper AB DiSpirito AA (1998) Cytochrome P460 genes from the methanotroph Methylococcus capsulatus Bath. J Bacteriol 180 : 6440 6445.
9. Bergmann DJ, Hooper AB Klotz MG (2005) Structure and sequence conservation of genes in the hao cluster of autotrophic ammonia-oxidizing bacteria: evidence for their evolutionary history. Appl Environment Microbiol 71 : 5371 5382.
10. Bodelier PLE Laanbroek HJ (2004) Nitrogen as a regulatory factor of methane oxidation in soils and sediments. FEMS Microbiol Ecol 47 : 265 277.
11. Brandes JA, Boctor NZ, Cody GD, Cooper BA, Hazen RM Yoder HS (1998) Abiotic nitrogen reduction on the early Earth. Nature 395 : 365 367.
12. Brandes JA, Devol AH Deutsch C (2007) New developments in the marine nitrogen cycle. Chem Rev 107 : 577 589.
13. Cabello P, Pino C, Olmo-Mira MF, Castillo F, Roldan MD Moreno-Vivian C (2004) Hydroxylamine Assimilation by Rhodobacter capsulatus E1F1: requirement of the hcp gene (hybrid cluster protein) located in the nitrate assimilation nas gene region for hydroxylamine reduction. J Biol Chem 279 : 45485 45494.
14. Canfield DE (1998) A new model for Proterozoic ocean chemistry. Nature 396 : 450 453.
15. Canfield D, Rosing M Bjerrum C (2006) Early anaerobic metabolisms. Philos Trans Roy Soc B: Biol Sci 361 : 1819 1836.
16. Cantera JJL Stein LY (2007a) Role of nitrite reductase in the ammonia-oxidizing pathway of Nitrosomonas europaea. Arch Microbiol 188 : 349 354.
17. Cantera JJL Stein LY (2007b) Molecular diversity of nitrite reductase genes (nirK) in nitrifying bacteria. Environment Microbiol 9 : 765 776.
18. Capone DG (2000) The marine microbial nitrogen cycle. Microbial Ecology of the Oceans (Kirchman DL, ed pp. 455 494. Wiley-Liss, New York, NY.
19. Capone DG Knapp AN (2007) Oceanography: a marine nitrogen cycle fix? Nature 445 : 159.
20. Capone DG, Popa R, Flood B Nealson KH (2006) Geochemistry: follow the nitrogen. Science 312 : 708 709.
21. Casciotti KL Ward BB (2005) Phylogenetic analysis of nitric oxide reductase gene homologues from aerobic ammonia-oxidizing bacteria. FEMS Microbiol Ecol 52 : 197 205.
22. Chain P, Lamerdin J, Larimer F et al 2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol 185 : 2759 2773.
23. Cho CMH, Yan T, Liu X, Wu L, Zhou J Stein LY (2006) Transcriptome of a Nitrosmonas europaea mutant with a disrupted nitrite reductase gene (nirK). Appl Environment Microbiol 72 : 4450 4454.
24. Colliver BB Stephenson T (2000) Production of nitrogen oxide and dinitrogen oxide by autotrophic nitrifiers. Biotechnol Adv 18 : 219 232.
25. Cruz-Ramos H, Crack J, Wu G, Hughes MN, Scott C, Thomson AJ, Green J Poole RK (2002) NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. EMBO J 21 : 3235 3244.
26. Dalsgaard T, Thamdrup B Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156 : 457 464.
27. Dore JE Karl DM (1996) Nitrification in the euphotic zone as a source for nitrite, nitrate, and nitrous oxide at Station ALOHA. Limnol Oceanogr 4 : 1619 1628.
28. Einsle O, Stach P, Messerschmidt A, Klimmek O, Simon J, Kroger A Kroneck PMH (2002) Crystallization and preliminary X-ray analysis of the membrane-bound cytochrome c nitrite reductase complex (NrfHA) from Wolinella succinogenes. Acta Crystallogr Section D 58 : 341 342.
29. Elmore BO, Bergmann DJ, Klotz MG Hooper AB (2007) Cytochromes P460 and c′-beta; A new family of high-spin cytochromes c. FEBS Lett 581 : 911 916.
30. 2 in the ocean. Nature 387 : 272.
31. Francis CA, Beman JM Kuypers MMM (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. The ISME J 1 : 19 27.
32. Galloway JN Cowling EB (2002) Reactive nitrogen and the world: 200 years of change. Ambio 31 : 64 71.
33. Garbeva P, Baggs EM Prosser JI (2007) Phylogeny of nitrite reductase (nirK) and nitric oxide reductase (norB) genes from Nitrosospira species isolated from soil. FEMS Microbiol Lett 266 : 83 89.
34. Garcia-Horsman JA, Barquera B, Rumbley J, Ma J Gennis RB (1994) The superfamily of heme-copper respiratory oxidases. J Bacteriol 176 : 5587 5600.
35. Gunsalus RP Wang H (2000) The nrfA and nirB nitrite reductase operons in Escherichia coli are expressed differently in response to nitrate than to nitrite. J Bacteriol 182 : 5813 5822.
36. Hanson RS Hanson TE (1996) Methanotrophic bacteria. Microbiol Rev 60 : 439 471.
37. Holmes AJ, Costello A, Lidstrom ME Murrell JC (1995) Evidence that particulate methane monooxygenase and ammonia monooxygenase may be evolutionarily related. FEMS Microbiol Lett 132 : 203 208.
38. Hooper AB, Arciero DM, Bergmann D Hendrich MP (2005) The oxidation of ammonia as an energy source in bacteria in respiration. Respiration in Archaea and Bacteria: Diversity of Procaryotic Respiratory Systems, Vol. 2 Zannoni Davide, ed pp. 121 147. Springer, Dordrecht, the Netherlands.
39. Houghton J, Ding Y, Griggs D, Noguer M van der Linden PJ (2001) Climate Change 2001: The Scientific Basis. Cambridge University Press, Cambridge, UK.
40. Igarashi N, Moriyama H, Fujiwara T, Fukumori Y Tanaka N (1997) The 2.8 A structure of hydroxylamine oxidoreductase from a nitrifying chemolithotrophic bacterium, Nitrosomonas europaea. Nat Struct Biol 4 : 276 284.
41. Iverson TM, Arciero DM, Hooper AB Rees DC (2001) High-resolution structures of the oxidized and reduced states of cytochrome c554 from Nitrosomonas europaea. J Biol Inorganic Chem 6 : 390 297.
42. Jetten MS, Cirpus I, Kartal B et al 2005) 1994-2004: 10 years of research on the anaerobic oxidation of ammonium. Biochem Soc Trans 33 : 119 133.
43. Kartal B, Kuypers MMM, Lavik G, Schalk J, Op den Camp HJM, Jetten MSM Strous M (2007) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environment Microbiol 9 : 635 642.
44. Kasting JF (1993) Earth's early atmosphere. Science 259 : 920 926.
45. King GM Schnell S (1994) Ammonium and nitrite inhibition of methane oxidation by Methylobacter albus BG8 and Methylosinus trichosporium OB3b at low methane concentrations. Appl Environment Microbiol 60 : 3508 3513.
46. Klotz MG Norton JM (1998) Multiple copies of ammonia monooxygenase (amo) operons have evolved under biased AT/GC mutational pressure in ammonia-oxidizing autotrophic bacteria. FEMS Microbiol Lett 168 : 303 311.
47. Klotz MG, Arp DJ, Chain PSG et al 2006) Complete genome sequence of the marine, chemolithoautotrophic, ammonia-oxidizing bacterium Nitrosococcus oceani ATCC 19707. Appl Environment Microbiol 72 : 6299 6315.
48. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB Stahl DA (2005) Isolation of an autotropic ammonia-oxidizing marine archaeon. Nature 437 : 543 546.
49. Koonin EV Martin W (2005) On the origin of genomes and cells within inorganic compartments. Trends Genetics 21 : 647.
50. Kowalchuk GA Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Ann Rev Microbiol 55 : 485 529.
51. Lawrence JG Hendrickson H (2005) Genome evolution in bacteria: order beneath chaos. Curr Opin Microbiol 8 : 572.
52. Lewis BL Landing WM (1992) The investigation of dissolved and suspended-particulate trace metal fractionation in the Black Sea. Marine Chem 40 : 105.
53. Lin JT Stewart V (1998) Nitrate assimilation in bacteria. Adv Microbial Physiol 39 : 1 30.
54. 2O by soil nitrifying bacteria. Nature 294 : 641 643.
55. Lontoh S, DiSpirito AA, Krema CL, Whittaker MR, Hooper AB Semrau JD (2000) Differential inhibition in vivo of ammonia monooxygenase, soluble methane monooxygenase and membrane-associated methane monooxygenase by phenylacetylene. Environment Microbiol 2 : 485 494.
56. Mancinelli RL McKay CP (1988) The evolution of nitrogen cycling. Origin Life Evol Biosphere 18 : 311 325.
57. McKay CP Navarro-González R (2001) The absence of nitrogen-fixing organelles due to timing of the nitrogen crisis. Symbiosis (Seckbach J, ed pp. 221 228. Springer, The Netherlands.
58. McLain JET Martens DA (2005) Nitrous oxide flux from soil and amino acid mineralization. Soil Biol Biochem 37 : 289 299.
59. Mohanty SR, Bodelier PLE, Floris V Conrad R (2006) Differential effects of nitrogenous fertilizers on methane-consuming microbes in rice field and forest soils. Appl Environment Microbiol 72 : 1346 1354.
60. Murrell JC Holmes AJ (1996) Molecular biology of particulate methane monooxygenase. Microbial Growth on C1 Compounds (Lidstrom ME Tabita FR, eds pp. 133 140. Kluwer Academic Publishers, the Netherlands.
61. Nakamura K Go N (2005) Function and molecular evolution of multicopper blue proteins. Cell Mol Life Sci 62 : 2050 2066.
62. Navarro-González R, McKay CP Mvondo DN (2001) A possible nitrogen crisis for Archaean life due to reduced nitrogen fixation by lightning. Nature 412 : 61 64.
63. 3 layer. J Geophysl Res 102 : 25519 25536.
64. Norton JM, Alzerreca JJ, Suwa Y Klotz MG (2002) Diversity of ammonia monooxygenase operon in autotrophic ammonia-oxidizing bacteria. Arch Microbiol 177 : 139 149.
65. Pino C, Olmo-Mira F, Cabello P, Martínez-Luque M, Castillo F, Roldán MD Moreno-Vivián C (2006) The assimilatory nitrate reduction system of the phototrophic bacterium Rhodobacter capsulatus E1F1. Biochem Soc Trans 34 : 127 129.
66. Postgate JR (1970) Biological nitrogen fixation. Nature 226 : 25 27.
67. Poulton SW, Fralick PW Canfield DE (2004) The transition to a sulphidic ocean [sim] 1.84 billion years ago. Nature 431 : 173.
68. Prosser JI (1989) Autotrophic nitrification in bacteria. Adv Microb Physiol 30 : 125 181.
69. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops H-P Wagner M (2000) Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environment Microbiol 66 : 5368 5382.
70. Raymond J, Siefert JL, Staples CR Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21 : 541 554.
71. Robertson GP, Paul EA Haarwood RR (2000) Greenhouse gases in intensive agriculture: contributions of individual gases to the radiative forceing of the atmosphere. Science 289 : 1922 1925.
72. Rodrigues ML, Oliveira T, Matias PM, Martins IC, Valente FM, Pereira IA Archer M (2006) Crystallization and preliminary structure determination of the membrane-bound complex cytochrome c nitrite reductase from Desulfovibrio vulgaris Hildenborough. Acta Crystallogr Sect F 62 : 565 568.
73. Schalk J, de Vries S, Kuenen JG Jetten MSM (2000) Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39 : 5405 5412.
74. 2 as oxidant is not inhibited by acetylene. Microbiology 147 : 2247 2253.
75. Schmidt I, van Spanning RJM Jetten MSM (2004) Denitrification and ammonia oxidation by Nitrosomonas europaea wild-type, and NirK- and NorB-deficient mutants. Microbiology 150 : 4107 4114.
76. Schmidt I, Steenbakkers PJM, op den Camp HJM, Schmidt K Jetten MSM (2004) Physiologic and proteomic evidence for a role of nitric oxide in biofilm formation by Nitrosomonas europaea and other ammonia oxidizers. J Bacteriol 186 : 2781 2788.
77. Shailaja MS, Narvekar PV, Alagarsamy R Naqvi SWA (2006) Nitrogen transformations as inferred from the activities of key enzymes in the Arabian Sea oxygen minimum zone. Deep-Sea Res I 53 : 960 970.
78. Simon J (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26 : 285 309.
79. Spirin V, Gelfand MS, Mironov AA Mirny LA (2006) A metabolic network in the evolutionary context: multiscale structure and modularity. PNAS 103 : 8774 8779.
80. Stein LY Yung YL (2003) Production, isotopic composition, and atmospheric fate of biologically produced nitrous oxide. Annual Rev Earth Planet Sci 31 : 329 356.
81. Stein LY, Arp DJ, Berube PM et al 2007) Whole-genome analysis of the ammonia-oxidizing bacterium, Nitrosomonas eutropha C91: implications for niche adaptation. Environment Microbiol 9 : 2993 3007.
82. Strous M, Pelletier E, Mangenot S et al 2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440 : 790.
83. 2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Commun Mass Spectr 17 : 738 745.
84. Teske A, Alm E, Regan J, Toze S, Rittmann B Stahl D (1994) Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria. J Bacteriol 176 : 6623 6630.
85. Van Spanning RJ, De Boer AP, Reijnders WN, Spiro S, Westerhoff HV, Stouthamer AH Van der Oost J (1995) Nitrite and nitric oxide reduction in Paracoccus denitrificans is under the control of NNR, a regulatory protein that belongs to the FNR family of transcriptional activators. FEBS Lett 360 : 151 154.
86. Wachtershauser G (2007) On the chemistry and evolution of the pioneer organism (review). Chem Biodiversity 4 : 584 602.
87. Ward BB O'Mullan GD (2002) Worldwide distribution of Nitrosococcus oceani, a marine ammonia-oxidizing gamma-proteobacterium, detected by PCR and sequencing of 16S rRNA and amoA genes. Appl Environment Microbiol 68 : 4153 4157.
88. Ward N, Larsen O, Sakwa J et al 2004) Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath). PLoS Biol 2 : e303.
89. Winogradsky S (1892) Contributions à la morphologie des organismes de la nitrification. Arch Sci Biol 1 : 88 37.
90. Wrage N, Velthof GL, van Beusichem ML Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 36 : 229 236.
91. Yung YL McElroy MC (1979) Fixation of nitrogen in the prebiotic atmosphere. Science 203 : 1002 1004.
92. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61 : 522 616.