Denitrifying Prokaryotes

Abstract

Denitrification is the dissimilatory reduction of nitrate to nitrogen gas. This respiratory process requires four enzymes that produce three obligatory intermediates prior to production of the terminal product. Denitrification is found in diverse array of microbes including members of both bacteria and archaea. However, no bacterium has been described that solely depends on denitrification as a form of energy generation. All denitrifiers, with one exception, are aerobes. Genome sequencing has provided a better appreciation of the distribution of denitrification genes among microbes. Complete denitrification, the reduction of nitrate to N2, is less frequent than partial denitrification among sequenced bacteria. Partial denitrification chains of nearly all possible arrangments have been found. This includes chains with only a single enzyme or discontinuous chains of two or more enzymes.

Nitrate reductase catalyzes the reduction of nitrate to nitrite and is used in a number of pathways other than denitrification; therefore, its distribution has not been a focus of this chapter. Nitrite reductase catalyzes the reduction of nitrite to nitric oxide and is the defining reaction of denitrification since it is the first step to produce a gaseous nitrogen oxide. There are two unrelated types of nitrite reductase, one of which has copper cofactors while the other contains heme-bound iron. The copper form has several different subtypes with N- and C-terminal extensions containing metal-binding sites. Some members of the Actinobacteria have a particularly large copper nitrite reductase with a membrane-bound domain of unknown function. Nitric oxide reductase catalyzes the reduction of nitric oxide to nitrous oxide. This enzyme is membrane bound and occurs in two subtypes referred to as cNor and qNor. The former receives electrons from cytochrome c while the latter carries an N-terminal extension allowing it to oxidize quinol. Nitrous oxide reductase is a soluble copper-containing enzyme with one of the copper centers, designated the CuZ center, being unique to this enzyme.

While most model denitrifiers use denitrification to support growth when oxygen is limiting, this may not be the case in all bacteria that contain genes encoding denitrification-associated nitrogen oxide reductases. Bacteria with partial chains consisting of a single enzyme may use that enzyme for alternative functions. For example, some Staphylococcus aureus subspecies aureus strains only contain nitric oxide reductase which is likely used for detoxification of nitric oxide. There are a number of bacteria which only contain nitrite reductase and the function of this enzyme is unclear in these organisms since its turnover will produce nitric oxide, which is toxic due to its reactivity with metal centers and other compounds.

Environmental studies have found denitrification genes are nearly universal in environments that receive some exposure to oxygen. Quantitative studies have found that the genes for nitrous oxide reductase are frequently underrepresented compared to other denitrification genes. While common in soil and aquatic environments, denitrifiers are also found in association with humans. Sequencing of both skin and oral microbiomes has revealed a significant number of denitrifiers, consistent with the occurrence of both nitrate and nitrite in these areas.

Keywords

Nitrate Reductase Horizontal Gene Transfer Nitrite Reductase Aerobic Denitrification Nitrous Oxide Reductase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Allison C, Macfarlane GT (1989) Dissimilatory nitrate reduction by Propionibacterium acnes. Appl Environ Microbiol 55:2899–2903PubMedGoogle Scholar
  2. Alvarez L, Bricio C, Gomez MJ, Berenguer J (2011) Lateral transfer of the denitrification pathway genes among Thermus thermophilus strains. Appl Environ Microbiol 77:1352–1358PubMedCrossRefGoogle Scholar
  3. Arai H, Kodama T, Igarashi Y (1997) Cascade regulation of the two CRP/FNR-related transcriptional regulators (ANR and DNR) and the denitrification enzymes in Pseudomonas aeruginosa. Mol Microbiol 25:1141–1148PubMedCrossRefGoogle Scholar
  4. Arai H, Mizutani M, Igarashi Y (2003) Transcriptional regulation of the nos genes for nitrous oxide reductase in Pseudomonas aeruginosa. Microbiology 149:29–36PubMedCrossRefGoogle Scholar
  5. Arnoux P, Sabaty M, Alric J, Frangioni B, Guigliarelli B, Adriano JM, Pignol D (2003) Structural and redox plasticity in the heterodimeric periplasmic nitrate reductase. Nat Struct Biol 10:928–934PubMedCrossRefGoogle Scholar
  6. Baek SH, Rajashekara G, Splitter GA, Shapleigh JP (2004) Denitrification genes regulate Brucella virulence in mice. J Bacteriol 186:6025–6031PubMedCrossRefGoogle Scholar
  7. Baek SH, Hartsock A, Shapleigh JP (2008) Agrobacterium tumefaciens C58 uses ActR and FnrN to control nirK and nor expression. J Bacteriol 190:78–86PubMedCrossRefGoogle Scholar
  8. Baker SC, Ferguson SJ, Ludwig B, Page MD, Richter OMH, van Spanning RJM (1998) Molecular genetics of the genus Paracoccus: metabolically versatile bacteria with bioenergetic flexibility. Microbiol Mol Biol Rev 62:1046–1078PubMedGoogle Scholar
  9. Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188:7344–7353PubMedCrossRefGoogle Scholar
  10. Barth KR, Isabella VM, Clark VL (2009) Biochemical and genomic analysis of the denitrification pathway within the genus Neisseria. Microbiology 155:4093–4103PubMedCrossRefGoogle Scholar
  11. Beaumont HJ, Lens SI, Reijnders WN, Westerhoff HV, van Spanning RJ (2004) Expression of nitrite reductase in Nitrosomonas europaea involves NsrR, a novel nitrite-sensitive transcription repressor. Mol Microbiol 54:148–158PubMedCrossRefGoogle Scholar
  12. Bell LC, Richardson DJ, Ferguson SJ (1990) Periplasmic and membrane-bound respiratory nitrate reductases in Thiosphaera pantotropha. The periplasmic enzyme catalyzes the first step in aerobic denitrification. FEBS Lett 265:85–87PubMedCrossRefGoogle Scholar
  13. Bergaust L, Shapleigh J, Frostegård Å, Bakken L (2008) Transcription and activities of NOx reductases in Agrobacterium tumefaciens: the influence of nitrate, nitrite and oxygen availability. Environ Microbiol 10:3070–3081PubMedCrossRefGoogle Scholar
  14. Bergaust L, Mao Y, Bakken LR, Frostegård Å (2011) Denitrification response patterns during the transition to anoxic respiration and posttranscriptional effects of suboptimal pH on nitrous oxide reductase in Paracoccus denitrificans. Appl Environ Microbiol 76:6387–6396CrossRefGoogle Scholar
  15. Bokranz M, Katz J, Schroder I, Roberton AM, Kroger A (1983) Energy metabolism and biosynthesis of Vibrio succinogenes growing with nitrate or nitrite as terminal electron acceptor. Arch Microbiol 135:36–41CrossRefGoogle Scholar
  16. Boulanger MJ, Murphy ME (2002) Crystal structure of the soluble domain of the major anaerobically induced outer membrane protein (AniA) from pathogenic Neisseria: a new class of copper-containing nitrite reductases. J Mol Biol 315:1111–1127PubMedCrossRefGoogle Scholar
  17. Brettar I, Christen R, Hofle MG (2002) Shewanella denitrificans sp. nov., a vigorously denitrifying bacterium isolated from the oxic-anoxic interface of the Gotland Deep in the central Baltic Sea. Int J Syst Evol Microbiol 52:2211–2217PubMedCrossRefGoogle Scholar
  18. Brondijk TH, Nilavongse A, Filenko N, Richardson DJ, Cole JA (2004) NapGH components of the periplasmic nitrate reductase of Escherichia coli K-12: location, topology and physiological roles in quinol oxidation and redox balancing. Biochem J 379:47–55PubMedCrossRefGoogle Scholar
  19. Brooijmans RJ, de Vos WM, Hugenholtz J (2009) Lactobacillus plantarum WCFS1 electron transport chains. Appl Environ Microbiol 75:3580–3585PubMedCrossRefGoogle Scholar
  20. Brown K, Prudencio M, Pereira AS, Besson S, Moura JJG, Moura I, Tegoni M, Cambillau C (2000) A novel type of catalytic copper cluster in nitrous oxide reductase. Nat Struct Biol 7:191–195PubMedCrossRefGoogle Scholar
  21. Bru D, Ramette A, Saby NP, Dequiedt S, Ranjard L, Jolivet C, Arrouays D, Philippot L (2011) Determinants of the distribution of nitrogen-cycling microbial communities at the landscape scale. ISME J 5:532–542PubMedCrossRefGoogle Scholar
  22. Brunekreef B, Holgate ST (2002) Air pollution and health. Lancet 360:1233–1242PubMedCrossRefGoogle Scholar
  23. Cabello P, Roldan MD, Moreno-Vivian C (2004) Nitrate reduction and the nitrogen cycle in archaea. Microbiology 150:3527–3546PubMedCrossRefGoogle Scholar
  24. Canfield DE, Glazer AN, Falkowski PG (2010) The evolution and future of Earth’s nitrogen cycle. Science 330:192–196PubMedCrossRefGoogle Scholar
  25. Carter JP, Hsiao YH, Spiro S, Richardson DJ (1995) Soil and sediment bacteria capable of aerobic nitrate respiration. Appl Environ Microbiol 61:2852–2858PubMedGoogle Scholar
  26. Castiglione N, Rinaldo S, Giardina G, Cutruzzola F (2009) The transcription factor DNR from Pseudomonas aeruginosa specifically requires nitric oxide and haem for the activation of a target promoter in Escherichia coli. Microbiology 155:2838–2844PubMedCrossRefGoogle Scholar
  27. Chain PS, Lang DM, Comerci DJ, Malfatti SA, Vergez LM, Shin M, Ugalde RA, Garcia E, Tolmasky ME (2011) Genome of Ochrobactrum anthropi ATCC 49188T, a versatile opportunistic pathogen and symbiont of several eukaryotic hosts. J Bacteriol 193:4274–4275Google Scholar
  28. Chang CK, Wu W (1986) The porphinedione structure of heme d 1: synthesis and spectral properties of model compounds of the prosthetic group of dissimilatory nitrite reductase. J Biol Chem 261:8593–8596PubMedGoogle Scholar
  29. Choudhary M, Zanhua X, Fu YX, Kaplan S (2007) Genome analyses of three strains of Rhodobacter sphaeroides: evidence of rapid evolution of chromosome II. J Bacteriol 189:1914–1921PubMedCrossRefGoogle Scholar
  30. Coyne S, Courvalin P, Galimand M (2010) Acquisition of multidrug resistance transposon Tn6061 and IS6100-mediated large chromosomal inversions in Pseudomonas aeruginosa clinical isolates. Microbiology 156:1448–1458PubMedCrossRefGoogle Scholar
  31. Cramm R, Siddiqui RA, Friedrich B (1997) Two isofunctional nitric oxide reductases in Alcaligenes eutrophus H16. J Bacteriol 179:6769–6777PubMedGoogle Scholar
  32. Cramm R, Pohlmann A, Friedrich B (1999) Purification and characterization of the single-component nitric oxide reductase from Ralstonia eutropha H16. FEBS Lett 460:6–10PubMedCrossRefGoogle Scholar
  33. Cua LS, Stein LY (2011) Effects of nitrite on ammonia-oxidizing activity and gene regulation in three ammonia-oxidizing bacteria. FEMS Microbiol Lett 319:169–175PubMedCrossRefGoogle Scholar
  34. Cuypers H, Viebrock-Sambale A, Zumft WG (1992) NosR, a membrane-bound regulatory component necessary for expression of nitrous oxide reductase in denitrifying Pseudomonas stutzeri. J Bacteriol 174:5332–5339PubMedGoogle Scholar
  35. de Boer AP, van der Oost J, Reijnders WN, Westerhoff HV, Stouthamer AH, van Spanning RJ (1996) Mutational analysis of the nor gene cluster which encodes nitric-oxide reductase from Paracoccus denitrificans. Eur J Biochem 242:592–600PubMedCrossRefGoogle Scholar
  36. de Vries S, Strampraad MJ, Lu S, Moenne-Loccoz P, Schroder I (2003) Purification and characterization of the MQH2:NO oxidoreductase from the hyperthermophilic archaeon Pyrobaculum aerophilum. J Biol Chem 278:35861–35868PubMedCrossRefGoogle Scholar
  37. Deiglmayr K, Philippot L, Hartwig UA, Kandeler E (2004) Structure and activity of the nitrate-reducing community in the rhizosphere of Lolium perenne and Trifolium repens under long-term elevated atmospheric pCO. FEMS Microbiol Ecol 49:445–454PubMedCrossRefGoogle Scholar
  38. Denariaz G, Payne WJ, Legall J (1989) A halophilic denitrifier, Bacillus halodenitrificans sp. nov. Int J Syst Bacteriol 39:145–151CrossRefGoogle Scholar
  39. Ellis MJ, Grossmann JG, Eady RR, Hasnain SS (2007) Genomic analysis reveals widespread occurrence of new classes of copper nitrite reductases. J Biol Inorg Chem 12:1119–1127PubMedCrossRefGoogle Scholar
  40. Enwall K, Throback IN, Stenberg M, Soderstrom M, Hallin S (2010) Soil resources influence spatial patterns of denitrifying communities at scales compatible with land management. Appl Environ Microbiol 76:2243–2250PubMedCrossRefGoogle Scholar
  41. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, Schreiber F, Dutilh BE, Zedelius J, de Beer D, Gloerich J, Wessels HJ, van Alen T, Luesken F, Wu ML, van de Pas-Schoonen KT, Op den Camp HJ, Janssen-Megens EM, Francoijs KJ, Stunnenberg H, Weissenbach J, Jetten MS, Strous M (2010) Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464:543–548PubMedCrossRefGoogle Scholar
  42. Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, Rodionov DA, Rodrigues JL, Saffarini DA, Serres MH, Spormann AM, Zhulin IB, Tiedje JM (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6:592–603PubMedCrossRefGoogle Scholar
  43. Fulop V, Moir JWB, Ferguson SJ, Hajdu J (1995) The anatomy of a bifunctional enzyme: structural basis for reduction of oxygen to water and synthesis of nitric oxide by cytochrome cd 1. Cell 81:369–377PubMedCrossRefGoogle Scholar
  44. Galyov EE, Brett PJ, DeShazer D (2010) Molecular insights into Burkholderia pseudomallei and Burkholderia mallei pathogenesis. Annu Rev Microbiol 64:495–517PubMedCrossRefGoogle Scholar
  45. Gavira M, Roldan MD, Castillo F, Moreno-Vivian C (2002) Regulation of nap gene expression and periplasmic nitrate reductase activity in the phototrophic bacterium Rhodobacter sphaeroides DSM158. J Bacteriol 184:1693–1702PubMedCrossRefGoogle Scholar
  46. Gayon U, Dupetit G (1882) Sur la fermentation des nitrates. C R Acad Sci 95:644–646Google Scholar
  47. Gayon U, Dupetit G (1886) Recherches sur la reduction des nitrates par les infinement petits. Mem Soc Sci Phys Nat Bordeaux Ser 3. 95:201–307Google Scholar
  48. Giardina G, Rinaldo S, Johnson KA, Di Matteo A, Brunori M, Cutruzzola F (2008) NO sensing in Pseudomonas aeruginosa: structure of the transcriptional regulator DNR. J Mol Biol 378:1002–1015PubMedCrossRefGoogle Scholar
  49. Glockner AB, Juengst A, Zumft WG (1993) Copper containing nitrite reductase from Pseudomonas aureofaciens is functional in a mutationally cytochrome cd 1-free background (nirs-) negative of Pseudomonas stutzeri. Arch Microbiol 160:18–26PubMedGoogle Scholar
  50. Godden JW, Turley S, Teller DC, Adman ET, Liu MY, Payne WJ, Legall J (1991) The 2.3 angstrom X-ray structure of nitrite reductase from Achromobacter cycloclastes. Science 253:438–442PubMedCrossRefGoogle Scholar
  51. Green SJ, Prakash O, Gihring TM, Akob DM, Jasrotia P, Jardine PM, Watson DB, Brown SD, Palumbo AV, Kostka JE (2010) Denitrifying bacteria isolated from terrestrial subsurface sediments exposed to mixed-waste contamination. Appl Environ Microbiol 76:3244–3254PubMedCrossRefGoogle Scholar
  52. Greenberg EP, Becker GE (1977) Nitrous oxide as end product of denitrification by strains of fluorescent pseudomonads. Can J Microbiol 23:903–907PubMedCrossRefGoogle Scholar
  53. Hafenbradl D, Keller M, Dirmeier R, Rachel R, Rossnagel P, Burggraf S, Huber H, Stetter KO (1996) Ferroglobus placidus gen. nov., sp. nov., A novel hyperthermophilic archaeum that oxidizes Fe2+ at neutral pH under anoxic conditions. Arch Microbiol 166:308–314PubMedCrossRefGoogle Scholar
  54. Haine V, Dozot M, Dornand J, Letesson JJ, De Bolle X (2006) NnrA is required for full virulence and regulates several Brucella melitensis denitrification genes. J Bacteriol 188:1615–1619PubMedCrossRefGoogle Scholar
  55. Hallin S, Jones CM, Schloter M, Philippot L (2009) Relationship between N-cycling communities and ecosystem functioning in a 50-year-old fertilization experiment. ISME J 3:597–605PubMedCrossRefGoogle Scholar
  56. Haltia T, Brown K, Tegoni M, Cambillau C, Saraste M, Mattila K, Djinovic-Carugo K (2003) Crystal structure of nitrous oxide reductase from Paracoccus denitrificans at 1.6 Å resolution. Biochem J 369:77–88PubMedCrossRefGoogle Scholar
  57. Harmsen HJ, Van Kuijk BL, Plugge CM, Akkermans AD, De Vos WM, Stams AJ (1998) Syntrophobacter fumaroxidans sp. nov., a syntrophic propionate-degrading sulfate-reducing bacterium. Int J Syst Bacteriol 48(Pt4):1383–1387PubMedCrossRefGoogle Scholar
  58. Harmsen M, Yang L, Pamp SJ, Tolker-Nielsen T (2011) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59:253–268Google Scholar
  59. Hartsock A, Shapleigh JP (2010) Identification, functional studies, and genomic comparisons of new members of the NnrR regulon in Rhodobacter sphaeroides. J Bacteriol 192:903–911PubMedCrossRefGoogle Scholar
  60. Hartsock A, Shapleigh JP (2011) Physiological roles for two periplasmic nitrate reductases in Rhodobacter sphaeroides 2.4.3 (ATCC 17025). J Bacteriol 193:6483–6489Google Scholar
  61. Hassett DJ, Cuppoletti J, Trapnell B, Lymar SV, Rowe JJ, Yoon SS, Hilliard GM, Parvatiyar K, Kamani MC, Wozniak DJ, Hwang SH, McDermott TR, Ochsner UA (2002) Anaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: rethinking antibiotic treatment strategies and drug targets. Adv Drug Deliv Rev 54:1425–1443PubMedCrossRefGoogle Scholar
  62. Henry S, Bru D, Stres B, Hallet S, Philippot L (2006) Quantitative detection of the nosZ gene, encoding nitrous oxide reductase, and comparison of the abundances of 16S rRNA, narG, nirK, and nosZ genes in soils. Appl Environ Microbiol 72:5181–5189PubMedCrossRefGoogle Scholar
  63. Heurlier K, Thomson MJ, Aziz N, Moir JW (2008) The nitric oxide (NO)-sensing repressor NsrR of Neisseria meningitidis has a compact regulon of genes involved in NO synthesis and detoxification. J Bacteriol 190:2488–2495PubMedCrossRefGoogle Scholar
  64. Hino T, Matsumoto Y, Nagano S, Sugimoto H, Fukumori Y, Murata T, Iwata S, Shiro Y (2010) Structural basis of biological N2O generation by bacterial nitric oxide reductase. Science 330:1666–1670PubMedCrossRefGoogle Scholar
  65. Ichiki H, Tanaka Y, Mochizuki K, Yoshimatsu K, Sakurai T, Fujiwara T (2001) Purification, characterization, and genetic analysis of Cu-containing dissimilatory nitrite reductase from a denitrifying halophilic archaeon, Haloarcula marismortui. J Bacteriol 183:4149–4156PubMedCrossRefGoogle Scholar
  66. Inatomi KI, Hochstein LI (1996) The purification and properties of a copper nitrite reductase from Haloferax denitrificans. Curr Microbiol 32:72–76CrossRefGoogle Scholar
  67. Iwata S, Ostermeier C, Ludwig B, Michel H (1995) Structure at 2.8 Å resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature 376:660–669PubMedCrossRefGoogle Scholar
  68. Jacobson F, Guo H, Olesen K, Okvist M, Neutze R, Sjolin L (2005) Structures of the oxidized and reduced forms of nitrite reductase from Rhodobacter sphaeroides 2.4.3 at high pH: changes in the interactions of the type 2 copper. Acta Crystallogr D Biol Crystallogr 61:1190–1198PubMedCrossRefGoogle Scholar
  69. Jain R, Shapleigh JP (2001) Characterization of nirV and a gene encoding a novel pseudoazurin in Rhodobacter sphaeroides 2.4.3. Microbiology 147:2505–2515PubMedGoogle Scholar
  70. Jeon CO, Park W, Padmanabhan P, DeRito C, Snape JR, Madsen EL (2003) Discovery of a bacterium, with distinctive dioxygenase, that is responsible for in situ biodegradation in contaminated sediment. Proc Natl Acad Sci USA 100:13591–13596PubMedCrossRefGoogle Scholar
  71. Jones CM, Hallin S (2010) Ecological and evolutionary factors underlying global and local assembly of denitrifier communities. ISME J 4:633–641PubMedCrossRefGoogle Scholar
  72. Jones CM, Welsh A, Throback IN, Dorsch P, Bakken LR, Hallin S (2011) Phenotypic and genotypic heterogeneity among closely related soil-borne N2 and N2O-producing Bacillus isolates harboring the nosZ gene. FEMS Microbiol Ecol 76:541–552PubMedCrossRefGoogle Scholar
  73. Kampschreur MJ, Picioreanu C, Tan N, Kleerebezem R, Jetten MS, van Loosdrecht MC (2007) Unraveling the source of nitric oxide emission during nitrification. Water Environ Res 79:2499–2509PubMedCrossRefGoogle Scholar
  74. Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions (supplement). DNA Res 3:185–209PubMedCrossRefGoogle Scholar
  75. Kaplan S, Eraso J, Roh JH (2005) Interacting regulatory networks in the facultative photosynthetic bacterium, Rhodobacter sphaeroides 2.4.1. Biochem Soc Trans 33:51–55PubMedCrossRefGoogle Scholar
  76. Keil D, Meyer A, Berner D, Poll C, Schutzenmeister A, Piepho HP, Vlasenko A, Philippot L, Schloter M, Kandeler E, Marhan S (2011) Influence of land-use intensity on the spatial distribution of N-cycling microorganisms in grassland soils. FEMS Microbiol Ecol 77:95–106PubMedCrossRefGoogle Scholar
  77. Kern M, Simon J (2008) Characterization of the NapGH quinol dehydrogenase complex involved in Wolinella succinogenes nitrate respiration. Mol Microbiol 69:1137–1152PubMedCrossRefGoogle Scholar
  78. Kim YJ, Ko IJ, Lee JM, Kang HY, Kim YM, Kaplan S, Oh JI (2007) Dominant role of the cbb 3 oxidase in regulation of photosynthesis gene expression through the PrrBA system in Rhodobacter sphaeroides 2.4.1. J Bacteriol 189:5617–5625PubMedCrossRefGoogle Scholar
  79. Kim M, Jeong SY, Yoon SJ, Cho SJ, Kim YH, Kim MJ, Ryu EY, Lee SJ (2008) Aerobic denitrification of Pseudomonas putida AD-21 at different C/N ratios. J Biosci Bioeng 106:498–502PubMedCrossRefGoogle Scholar
  80. Kim SW, Fushinobu S, Zhou S, Wakagi T, Shoun H (2009) Eukaryotic nirK genes encoding copper-containing nitrite reductase: originating from the protomitochondrion? Appl Environ Microbiol 75:2652–2658PubMedCrossRefGoogle Scholar
  81. Kong HH (2011) Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med 17:320–328PubMedCrossRefGoogle Scholar
  82. Korner H, Zumft WG (1989) Expression of denitrification enzymes in response to the dissolved oxygen and respiratory substrate in continuous culture of Pseudomonas stutzeri. Appl Environ Microbiol 55:1670–1676PubMedGoogle Scholar
  83. Korner H, Sofia HJ, Zumft WG (2003) Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 27:559–592PubMedCrossRefGoogle Scholar
  84. Kwiatkowski A, Shapleigh JP (1996) Requirement of nitric oxide for induction of genes whose products are involved in nitric oxide metabolism in Rhodobacter sphaeroides 2.4.3. J Biol Chem 271:24382–24388PubMedCrossRefGoogle Scholar
  85. Lam Y, Nicholas DJD (1969) A nitrite reductase with cytochrome oxidase activity from Paracoccus denitrificans. Biochim Biophys Acta 180:459–472PubMedCrossRefGoogle Scholar
  86. Laratta WP, Choi PS, Tosques IE, Shapleigh JP (2002) Involvement of the PrrB/PrrA two-component system in nitrite respiration in Rhodobacter sphaeroides 2.4.3: evidence for transcriptional regulation. J Bacteriol 184:3521–3529PubMedCrossRefGoogle Scholar
  87. Laver JR, Stevanin TM, Messenger SL, Lunn AD, Lee ME, Moir JW, Poole RK, Read RC (2010) Bacterial nitric oxide detoxification prevents host cell S-nitrosothiol formation: a novel mechanism of bacterial pathogenesis. FASEB J 24:286–295PubMedCrossRefGoogle Scholar
  88. Lim SK, Kim SJ, Cha SH, Oh YK, Rhee HJ, Kim MS, Lee JK (2009) Complete genome sequence of Rhodobacter sphaeroides KD131. J Bacteriol 191:1118–1119PubMedCrossRefGoogle Scholar
  89. Liu B, Morkved PT, Frostegård Å, Bakken LR (2010) Denitrification gene pools, transcription and kinetics of NO, N2O and N2 production as affected by soil pH. FEMS Microbiol Ecol 72:407–417PubMedCrossRefGoogle Scholar
  90. Lovley DR, Phillips EJ (1988) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54:1472–1480PubMedGoogle Scholar
  91. Lundberg JO, Govoni M (2004) Inorganic nitrate is a possible source for systemic generation of nitric oxide. Free Radic Biol Med 37:395–400PubMedCrossRefGoogle Scholar
  92. Lundberg JO, Weitzberg E, Cole JA, Benjamin N (2004) Nitrate, bacteria and human health. Nat Rev Microbiol 2:593–602PubMedCrossRefGoogle Scholar
  93. Mackenzie C, Choudhary M, Larimer FW, Predki PF, Stilwagen S, Armitage JP, Barber RD, Donohue TJ, Hosler JP, Newman JE, Shapleigh JP, Sockett RE, Zeilstra-Ryalls J, Kaplan S (2001) The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosyn Res 70:19–41PubMedCrossRefGoogle Scholar
  94. MacPherson IS, Murphy ME (2007) Type-2 copper-containing enzymes. Cell Mol Life Sci 64:2887–2899PubMedCrossRefGoogle Scholar
  95. Mahne I, Tiedje JM (1995) Criteria and methodology for identifying respiratory denitrifiers. Appl Environ Microbiol 61:1110–1115PubMedGoogle Scholar
  96. Mancinelli RL, Hochstein LI (1986) The occurrence of denitrification in extremely halophilic bacteria. FEMS Microbiol Lett 35:55–58PubMedCrossRefGoogle Scholar
  97. Martinez-Espinosa RM, Cole JA, Richardson DJ, Watmough NJ (2011) Enzymology and ecology of the nitrogen cycle. Biochem Soc Trans 39:175–178PubMedCrossRefGoogle Scholar
  98. Matsubara T, Zumft WG (1982) Identification of a copper protein as part of the nitrous oxide-reducing system in nitrite respiring (denitrifying) pseudomonads. Arch Microbiol 132:322–328CrossRefGoogle Scholar
  99. McClain ME, Boyer EW, Dent CL, Gergel SE, Grimm NB, Groffman PM, Hart SC, Harvey JW, Johnston CA, Mayorga E, McDowell WH, Pinay G (2003) Biogeochemical hot spots and hot moments at the interface of terrestrial and aquatic ecosystems. Ecosystems 6:301–312CrossRefGoogle Scholar
  100. McEwan AG, Jackson JB, Ferguson SJ (1984) Rationalisation of properties of nitrate reductases in Rhodopseudomonas capsulata. Arch Microbiol 137:344–349CrossRefGoogle Scholar
  101. Medigue C, Krin E, Pascal G, Barbe V, Bernsel A, Bertin PN, Cheung F, Cruveiller S, D'Amico S, Duilio A, Fang G, Feller G, Ho C, Mangenot S, Marino G, Nilsson J, Parrilli E, Rocha EP, Rouy Z, Sekowska A, Tutino ML, Vallenet D, von Heijne G, Danchin A (2005) Coping with cold: the genome of the versatile marine Antarctica bacterium Pseudoalteromonas haloplanktis TAC125. Genome Res 15:1325–1335PubMedCrossRefGoogle Scholar
  102. Mellies J, Jose J, Meyer TF (1997) The Neisseria gonorrhoeae gene aniA encodes an inducible nitrite reductase. Mol Gen Genet 256:525–532PubMedCrossRefGoogle Scholar
  103. Mesa S, Velasco L, Manzanera ME, Delgado MJ, Bedmar EJ (2002) Characterization of the norCBQD genes, encoding nitric oxide reductase, in the nitrogen fixing bacterium Bradyrhizobium japonicum. Microbiology 148:3553–3560PubMedGoogle Scholar
  104. Mesa S, Hauser F, Friberg M, Malaguti E, Fischer HM, Hennecke H (2008) Comprehensive assessment of the regulons controlled by the FixLJ-FixK2-FixK1 cascade in Bradyrhizobium japonicum. J Bacteriol 190:6568–6579PubMedCrossRefGoogle Scholar
  105. Michalski W, Nicholas DJD (1988) Identification of two new denitrifying strains of Rhodobacter sphaeroides. FEMS Microbiol Lett 52:239–244CrossRefGoogle Scholar
  106. Mowbray M, McLintock S, Weerakoon R, Lomatschinsky N, Jones S, Rossi AG, Weller RB (2009) Enzyme-independent NO stores in human skin: quantification and influence of UV radiation. J Invest Dermatol 129:834–842PubMedCrossRefGoogle Scholar
  107. Nakagawa S, Takai K, Inagaki F, Horikoshi K, Sako Y (2005) Nitratiruptor tergarcus gen. nov., sp. nov. and Nitratifractor salsuginis gen. nov., sp. nov., nitrate-reducing chemolithoautotrophs of the epsilon-Proteobacteria isolated from a deep-sea hydrothermal system in the Mid-Okinawa trough. Int J Syst Evol Microbiol 55:925–933PubMedCrossRefGoogle Scholar
  108. Nakagawa S, Takaki Y, Shimamura S, Reysenbach AL, Takai K, Horikoshi K (2007) Deep-sea vent epsilon-proteobacterial genomes provide insights into emergence of pathogens. Proc Natl Acad Sci USA 104:12146–12150PubMedCrossRefGoogle Scholar
  109. Nakanishi Y, Zhou S, Kim SW, Fushinobu S, Maruyama J, Kitamoto K, Wakagi T, Shoun H (2010) A eukaryotic copper-containing nitrite reductase derived from a NirK homolog gene of Aspergillus oryzae. Biosci Biotechnol Biochem 74:984–991PubMedCrossRefGoogle Scholar
  110. Neidhardt FC, Ingraham JL, Schaechter M (1990) Physiology of the bacterial cell: a molecular approach. Sinauer Associates, SunderlandGoogle Scholar
  111. Nojiri M, Xie Y, Inoue T, Yamamoto T, Matsumura H, Kataoka K, Deligeer K, Yamaguchi YK, Suzuki S (2007) Structure and function of a hexameric copper-containing nitrite reductase. Proc Natl Acad Sci USA 104:4315–4320PubMedCrossRefGoogle Scholar
  112. Nojiri M, Koteishi H, Nakagami T, Kobayashi K, Inoue T, Yamaguchi K, Suzuki S (2009a) Structural basis of inter-protein electron transfer for nitrite reduction in denitrification. Nature 462:117–120PubMedCrossRefGoogle Scholar
  113. Nojiri M, Shirota F, Hira D, Suzuki S (2009b) Expression, purification, crystallization and preliminary X-ray diffraction analysis of the soluble domain of PPA0092, a putative nitrite reductase from Propionibacterium acnes. Acta Crystallogr Sect F Struct Biol Cryst Commun 65:123–127PubMedCrossRefGoogle Scholar
  114. Nurizzo D, Silvestrini MC, Mathieu M, Cutruzzola F, Bourgeois D, Fulop V, Hajdu J, Brunori M, Tegoni M, Cambillau C (1997) N-terminal arm exchange is observed in the 2.15 Å crystal structure of oxidized nitrite reductase from Pseudomonas aeruginosa. Structure 15:1157–1171CrossRefGoogle Scholar
  115. Parales RE, Parales JV, Pelletier DA, Ditty JL (2008) Diversity of microbial toluene degradation pathways. Adv Appl Microbiol 64:1–73PubMedCrossRefGoogle Scholar
  116. Paraskevopoulos K, Antonyuk SV, Sawers RG, Eady RR, Hasnain SS (2006) Insight into catalysis of nitrous oxide reductase from high-resolution structures of resting and inhibitor-bound enzyme from Achromobacter cycloclastes. J Mol Biol 362:55–65PubMedCrossRefGoogle Scholar
  117. Payne WJ (1981) Denitrification. Wiley, New YorkGoogle Scholar
  118. Payne WJ, Grant MA, Shapleigh JP, Hoffman P (1982) Nitrogen oxide reduction in Wolinella succinogenes and Campylobacter species. J Bacteriol 152:915–918PubMedGoogle Scholar
  119. Philippot L, Cuhel J, Saby NP, Cheneby D, Chronakova A, Bru D, Arrouays D, Martin-Laurent F, Simek M (2009) Mapping field-scale spatial patterns of size and activity of the denitrifier community. Environ Microbiol 11:1518–1526PubMedCrossRefGoogle Scholar
  120. Picardeau M, Bulach DM, Bouchier C, Zuerner RL, Zidane N, Wilson PJ, Creno S, Kuczek ES, Bommezzadri S, Davis JC, McGrath A, Johnson MJ, Boursaux-Eude C, Seemann T, Rouy Z, Coppel RL, Rood JI, Lajus A, Davies JK, Medigue C, Adler B (2008) Genome sequence of the saprophyte Leptospira biflexa provides insights into the evolution of Leptospira and the pathogenesis of leptospirosis. PLoS One 3:e1607PubMedCrossRefGoogle Scholar
  121. Pukall R, Gehrich-Schroter G, Lapidus A, Nolan M, Glavina Del Rio T, Lucas S, Chen F, Tice H, Pitluck S, Cheng JF, Copeland A, Saunders E, Brettin T, Detter JC, Bruce D, Goodwin L, Pati A, Ivanova N, Mavromatis K, Ovchinnikova G, Chen A, Palaniappan K, Land M, Hauser L, Chang YJ, Jeffries CD, Chain P, Goker M, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk HP, Han C (2009) Complete genome sequence of Jonesia denitrificans type strain (Prevot 55134). Stand Genomic Sci 1:262–269PubMedCrossRefGoogle Scholar
  122. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125PubMedCrossRefGoogle Scholar
  123. Rendulic S, Jagtap P, Rosinus A, Eppinger M, Baar C, Lanz C, Keller H, Lambert C, Evans KJ, Goesmann A, Meyer F, Sockett RE, Schuster SC (2004) A predator unmasked: life cycle of Bdellovibrio bacteriovorus from a genomic perspective. Science 303:689–692PubMedCrossRefGoogle Scholar
  124. Rhee SK, Jeon CO, Bae JW, Kim K, Song JJ, Kim JJ, Lee SG, Kim HI, Hong SP, Choi YH, Kim SM, Sung MH (2002) Characterization of Symbiobacterium toebii, an obligate commensal thermophile isolated from compost. Extremophiles 6:57–64PubMedCrossRefGoogle Scholar
  125. Richardson DJ, Berks BC, Russell DA, Spiro S, Taylor CJ (2001) Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci 58:165–178PubMedCrossRefGoogle Scholar
  126. Richardson D, Felgate H, Watmough N, Thomson A, Baggs E (2009) Mitigating release of the potent greenhouse gas N2O from the nitrogen cycle – could enzymic regulation hold the key? Trends Biotechnol 27:388–397PubMedCrossRefGoogle Scholar
  127. Rinaldo S, Giardina G, Castiglione N, Stelitano V, Cutruzzola F (2011) The catalytic mechanism of Pseudomonas aeruginosa cd 1 nitrite reductase. Biochem Soc Trans 39:195–200PubMedCrossRefGoogle Scholar
  128. Risgaard-Petersen N, Langezaal AM, Ingvardsen S, Schmid MC, Jetten MS, Op den Camp HJ, Derksen JW, Pina-Ochoa E, Eriksson SP, Nielsen LP, Revsbech NP, Cedhagen T, van der Zwaan GJ (2006) Evidence for complete denitrification in a benthic foraminifer. Nature 443:93–96PubMedCrossRefGoogle Scholar
  129. Rodionov DA, Dubchak IL, Arkin AP, Alm EJ, Gelfand MS (2005) Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput Biol 1:e55PubMedCrossRefGoogle Scholar
  130. Roop RM 2nd, Gaines JM, Anderson ES, Caswell CC, Martin DW (2009) Survival of the fittest: how Brucella strains adapt to their intracellular niche in the host. Med Microbiol Immunol 198:221–238PubMedCrossRefGoogle Scholar
  131. Sanford RA, Cole JR, Tiedje JM (2002) Characterization and description of Anaeromyxobacter dehalogenans gen. nov., sp. nov., an aryl-halorespiring facultative anaerobic myxobacterium. Appl Environ Microbiol 68:893–900PubMedCrossRefGoogle Scholar
  132. Saraste M, Castresana J (1994) Cytochrome oxidase evolved by tinkering with denitrification enzymes. FEBS Lett 341:1–4PubMedCrossRefGoogle Scholar
  133. Sawada E, Satoh T (1980) Periplasmic location of dissimilatory nitrate and nitrite reductases in a denitrifying phototrophic bacterium, Rhodopseudomonas sphaeroides forma sp. denitrificans. Plant Cell Physiol 21:205–210Google Scholar
  134. Schlag S, Fuchs S, Nerz C, Gaupp R, Engelmann S, Liebeke M, Lalk M, Hecker M, Gotz F (2008) Characterization of the oxygen-responsive NreABC regulon of Staphylococcus aureus. J Bacteriol 190:7847–7858PubMedCrossRefGoogle Scholar
  135. Schwarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460:839–847PubMedCrossRefGoogle Scholar
  136. Sears HJ, Sawers G, Berks BC, Ferguson SJ, Richardson DJ (2000) Control of periplasmic nitrate reductase gene expression (napEDABC) from Paracoccus pantotrophus in response to oxygen and carbon substrates. Microbiology 146:2977–2985PubMedGoogle Scholar
  137. Shapleigh JP (2011) Oxygen control of nitrogen oxide respiration, focusing on alpha-proteobacteria. Biochem Soc Trans 39:179–183PubMedCrossRefGoogle Scholar
  138. Sievert SM, Scott KM, Klotz MG, Chain PS, Hauser LJ, Hemp J, Hugler M, Land M, Lapidus A, Larimer FW, Lucas S, Malfatti SA, Meyer F, Paulsen IT, Ren Q, Simon J (2008) Genome of the epsilonproteobacterial chemolithoautotroph Sulfurimonas denitrificans. Appl Environ Microbiol 74:1145–1156PubMedCrossRefGoogle Scholar
  139. Simek M, Cooper JE (2002) The influence of soil pH on denitrification: progress towards the understanding of this interaction over the last 50 years. Eur J Soil Sci 53:345–354CrossRefGoogle Scholar
  140. Simon J (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26:285–309PubMedCrossRefGoogle Scholar
  141. Simon J, Einsle O, Kroneck PM, Zumft WG (2004) The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase. FEBS Lett 569:7–12PubMedCrossRefGoogle Scholar
  142. Stevanin TM, Laver JR, Poole RK, Moir JW, Read RC (2007) Metabolism of nitric oxide by Neisseria meningitidis modifies release of NO-regulated cytokines and chemokines by human macrophages. Microbes Infect 9:981–987PubMedCrossRefGoogle Scholar
  143. Strohm TO, Griffin B, Zumft WG, Schink B (2007) Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73:1420–1424PubMedCrossRefGoogle Scholar
  144. Suharti, Heering HA, de Vries S (2004) NO reductase from Bacillus azotoformans is a bifunctional enzyme accepting electrons from menaquinol and a specific endogenous membrane-bound cytochrome c 551. Biochemistry 43:13487–13495Google Scholar
  145. Suharti, Strampraad MJF, Schroder I, de VS (2001) A novel copper A containing menaquinol NO reductase from Bacillus azotoformans. Biochemistry 40:2632–2639Google Scholar
  146. Swem LR, Elsen S, Bird TH, Swem DL, Koch HG, Myllykallio H, Daldal F, Bauer CE (2001) The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus. J Mol Biol 309:121–138PubMedCrossRefGoogle Scholar
  147. Tabata A, Yamamoto I, Matsuzaki M, Satoh T (2005) Differential regulation of periplasmic nitrate reductase gene (napKEFDABC) expression between aerobiosis and anaerobiosis with nitrate in a denitrifying phototroph Rhodobacter sphaeroides f. sp. denitrificans. Arch Microbiol 184:108–116PubMedCrossRefGoogle Scholar
  148. Tavares P, Pereira AS, Moura JJ, Moura I (2006) Metalloenzymes of the denitrification pathway. J Inorg Biochem 100:2087–2100PubMedCrossRefGoogle Scholar
  149. Thomsen JK, Geest T, Cox RP (1994) Mass-spectrometric studies of the effect of pH on the accumulation of intermediates in denitrification by Paracoccus denitrificans. Appl Environ Microbiol 60:536–541PubMedGoogle Scholar
  150. Tocheva EI, Rosell FI, Mauk AG, Murphy ME (2004) Side-on copper-nitrosyl coordination by nitrite reductase. Science 304:867–870PubMedCrossRefGoogle Scholar
  151. Toffanin A, Wu Q, Maskus M, Casella S, Abruña HD, Shapleigh JP (1996) Characterization of the gene encoding nitrite reductase and the physiological consequences of its expression in the nondenitrifying Rhizobium “hedysari” strain HCNT1. Appl Environ Microbiol 62:4019–4025PubMedGoogle Scholar
  152. Torres MJ, Bueno E, Mesa S, Bedmar EJ, Delgado MJ (2011) Emerging complexity in the denitrification regulatory network of Bradyrhizobium japonicum. Biochem Soc Trans 39:284–288PubMedCrossRefGoogle Scholar
  153. Tosques IE, Kwiatkowski AV, Shi J, Shapleigh JP (1997) Characterization and regulation of the gene encoding nitrite reductase in Rhodobacter sphaeroides 2.4.3. J Bacteriol 179:1090–1095PubMedGoogle Scholar
  154. Toyofuku M, Nomura N, Fujii T, Takaya N, Maseda H, Sawada I, Nakajima T, Uchiyama H (2007) Quorum sensing regulates denitrification in Pseudomonas aeruginosa PAO1. J Bacteriol 189:4969–4972PubMedCrossRefGoogle Scholar
  155. Tunbridge AJ, Stevanin TM, Lee M, Marriott HM, Moir JW, Read RC, Dockrell DH (2006) Inhibition of macrophage apoptosis by Neisseria meningitidis requires nitric oxide detoxification mechanisms. Infect Immun 74:729–733PubMedCrossRefGoogle Scholar
  156. Ueda K, Yamashita A, Ishikawa J, Shimada M, Watsuji TO, Morimura K, Ikeda H, Hattori M, Beppu T (2004) Genome sequence of Symbiobacterium thermophilum, an uncultivable bacterium that depends on microbial commensalism. Nucleic Acids Res 32:4937–4944PubMedCrossRefGoogle Scholar
  157. van den Heuvel RN, van der Biezen E, Jetten MS, Hefting MM, Kartal B (2010) Denitrification at pH 4 by a soil-derived Rhodanobacter-dominated community. Environ Microbiol 12:3264–3271PubMedCrossRefGoogle Scholar
  158. van der Oost J, de Boer APN, De Gier J-WL, Zumft WG, Stouthamer AH, van Spanning RJM (1994) The heme-copper oxidase family consists of three distinct types of oxidases and is related to nitric oxide reductase. FEMS Microbiol Lett 121:1–9PubMedCrossRefGoogle Scholar
  159. Van Spanning RJ, Houben E, Reijnders WN, Spiro S, Westerhoff HV, Saunders N (1999) Nitric oxide is a signal for NNR-mediated transcription activation in Paracoccus denitrificans. J Bacteriol 181:4129–4132PubMedGoogle Scholar
  160. van Spanning R, Richardson D, Ferguson S (2007) Introduction to the biochemistry and molecular biology of denitrification. In: Bothe H, Ferguson S, Newton W (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 3–21CrossRefGoogle Scholar
  161. Velasco L, Mesa S, Xu CA, Delgado MJ, Bedmar EJ (2004) Molecular characterization of nosRZDFYLX genes coding for denitrifying nitrous oxide reductase of Bradyrhizobium japonicum. Antonie Van Leeuwenhoek 85:229–235PubMedCrossRefGoogle Scholar
  162. Verbaendert I, Boon N, De Vos P, Heylen K (2011) Denitrification is a common feature among members of the genus Bacillus. Syst Appl Microbiol 34:385–391PubMedCrossRefGoogle Scholar
  163. Vidon P, Allan C, Burns D, Duval TP, Gurwick N, Inamdar S, Lowrance R, Okay J, Scott D, Sebestyen S (2010) Hot spots and hot moments in riparian zones: potential for improved water quality management. J Am Water Resour Assoc 46:278–298CrossRefGoogle Scholar
  164. Volkl P, Huber R, Drobner E, Rachel R, Burggraf S, Trincone A, Stetter KO (1993) Pyrobaculum aerophilum sp. nov., a novel nitrate-reducing hyperthermophilic archaeum. Appl Environ Microbiol 59:2918–2926PubMedGoogle Scholar
  165. Vollack K, Zumft W (2001) Nitric oxide signaling and transcriptional control of denitrification genes in Pseudomonas stutzeri. J Bacteriol 183:2516–2526PubMedCrossRefGoogle Scholar
  166. Volland S, Rachinger M, Strittmatter A, Daniel R, Gottschalk G, Meyer O (2011) Complete genome sequences of the chemolithoautotrophic strains Oligotropha carboxidovorans OM4 and OM5. J Bacteriol 193:5043Google Scholar
  167. Vorholt JA, Hafenbradl D, Stetter KO, Thauer RK (1997) Pathways of autotrophic CO2 fixation and of dissimilatory nitrate reduction to N2O in Ferroglobus placidus. Arch Microbiol 167:19–23PubMedCrossRefGoogle Scholar
  168. Voskuil MI, Bartek IL, Visconti K, Schoolnik GK (2011) The response of Mycobacterium tuberculosis to reactive oxygen and nitrogen species. Front Microbiol 2:105PubMedCrossRefGoogle Scholar
  169. Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PS, Chan PP, Gollabgir A, Hemp J, Hugler M, Karr EA, Konneke M, Shin M, Lawton TJ, Lowe T, Martens-Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107:8818–8823PubMedCrossRefGoogle Scholar
  170. Wan C, Yang X, Lee DJ, Du M, Wan F, Chen C (2011) Aerobic denitrification by novel isolated strain using NO2–N as nitrogen source. Bioresour Technol 102:7244–7248PubMedCrossRefGoogle Scholar
  171. Wattam AR, Williams KP, Snyder EE, Almeida NF Jr, Shukla M, Dickerman AW, Crasta OR, Kenyon R, Lu J, Shallom JM, Yoo H, Ficht TA, Tsolis RM, Munk C, Tapia R, Han CS, Detter JC, Bruce D, Brettin TS, Sobral BW, Boyle SM, Setubal JC (2009) Analysis of ten Brucella genomes reveals evidence for horizontal gene transfer despite a preferred intracellular lifestyle. J Bacteriol 191:3569–3579PubMedCrossRefGoogle Scholar
  172. Wharton DC, Gibson QC (1976) Cytochrome oxidase from Pseudomonas aeruginosa IV. Reaction with oxygen and carbon monoxide. Biochim Biophys Acta 292:611–620Google Scholar
  173. Wu ML, Ettwig KF, Jetten MS, Strous M, Keltjens JT, van Niftrik L (2011) A new intra-aerobic metabolism in the nitrite-dependent anaerobic methane-oxidizing bacterium Candidatus “Methylomirabilis oxyfera”. Biochem Soc Trans 39:243–248PubMedCrossRefGoogle Scholar
  174. Wunsch P, Zumft WG (2005) Functional domains of NosR, a novel transmembrane iron-sulfur flavoprotein necessary for nitrous oxide respiration. J Bacteriol 187:1992–2001PubMedCrossRefGoogle Scholar
  175. Xie SG, Zhang XJ, Wang ZS (2003) Temperature effect on aerobic denitrification and nitrification. J Environ Sci (China) 15:669–673Google Scholar
  176. Yagi JM, Sims D, Brettin T, Bruce D, Madsen EL (2009) The genome of Polaromonas naphthalenivorans strain CJ2, isolated from coal tar-contaminated sediment, reveals physiological and metabolic versatility and evolution through extensive horizontal gene transfer. Environ Microbiol 11:2253–2270PubMedCrossRefGoogle Scholar
  177. Ye RW, Arunakumari A, Averill BA, Tiedje JM (1992) Mutants of Pseudomonas fluorescens deficient in dissimilatory nitrite reduction are also altered in nitric oxide reduction. J Bacteriol 174:2560–2564PubMedGoogle Scholar
  178. Yoshimatsu K, Sakurai T, Fujiwara T (2000) Purification and characterization of dissimilatory nitrate reductase from a denitrifying halophilic archaeon, Haloarcula marismortui. FEBS Lett 470:216–220PubMedCrossRefGoogle Scholar
  179. Yoshinari T (1980) N2O reduction by Vibrio succinogenes. Appl Environ Microbiol 39:81–84PubMedGoogle Scholar
  180. Zumft WG (1997) Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616PubMedGoogle Scholar
  181. Zumft WG, Kroneck PM (2006) Respiratory transformation of nitrous oxide (N2O) to dinitrogen by bacteria and archaea. Adv Microb Physiol 52:107–227CrossRefGoogle Scholar
  182. Zumft WG, Matsubara T (1982) A novel kind of multi-copper protein as terminal oxidoreductase of nitrous oxide respiration in Pseudomonas perfectomarinus. FEBS Lett 148:107–112CrossRefGoogle Scholar
  183. Zumft WG, Braun C, Cuypers H (1994) Nitric oxide reductase from Pseudomonas stutzeri: primary structure and gene organization of a novel bacterial cytochrome bc complex. Eur J Biochem 219:481–490PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Department of MicrobiologyCornell UniversityIthacaUSA

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