1887

Abstract

Global warming is moving more and more into the public consciousness. Besides the commonly mentioned carbon dioxide and methane, nitrous oxide (NO) is a powerful greenhouse gas in addition to its contribution to depletion of stratospheric ozone. The increasing concern about NO emission has focused interest on underlying microbial energy-converting processes and organisms harbouring NO reductase (NosZ), such as denitrifiers and ammonifiers of nitrate and nitrite. Here, the epsilonproteobacterial model organism is investigated with regard to its capacity to produce and consume NO during growth by anaerobic nitrate ammonification. This organism synthesizes an unconventional cytochrome nitrous oxide reductase (NosZ), which is encoded by the first gene of an atypical gene cluster. However, lacks a nitric oxide (NO)-producing nitrite reductase of the NirS- or NirK-type as well as an NO reductase of the Nor-type. Using a robotized incubation system, the wild-type strain and suitable mutants of that either produced or lacked NosZ were analysed as to their production of NO, NO and N in both nitrate-sufficient and nitrate-limited growth medium using formate as electron donor. It was found that cells growing in nitrate-sufficient medium produced small amounts of NO, which derived from nitrite and, most likely, from the presence of NO. Furthermore, cells employing NosZ were able to reduce NO to N. This reaction, which was fully inhibited by acetylene, was also observed after adding NO to the culture headspace. The results indicate that cells are competent in NO and N production despite being correctly grouped as respiratory nitrate ammonifiers. NO production is assumed to result from NO detoxification and nitrosative stress defence, while NO serves as a terminal electron acceptor in anaerobic respiration. The ecological implications of these findings are discussed.

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2014-08-01
2020-09-28
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References

  1. Baar C., Eppinger M., Raddatz G., Simon J., Lanz C., Klimmek O., Nandakumar R., Gross R., Rosinus A..& other authors ( 2003;). Complete genome sequence and analysis of Wolinella succinogenes. Proc Natl Acad Sci U S A100:11690–11695 [CrossRef][PubMed]
    [Google Scholar]
  2. 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 Microbiol10:3070–3081 [CrossRef][PubMed]
    [Google Scholar]
  3. Bergaust L., van Spanning R. J. M., Frostegård Å., Bakken L. R..( 2012;). Expression of nitrous oxide reductase in Paracoccus denitrificans is regulated by oxygen and nitric oxide through FnrP and NNR. Microbiology158:826–834 [CrossRef][PubMed]
    [Google Scholar]
  4. Bleakley B. H., Tiedje J. M..( 1982;). Nitrous oxide production by organisms other than nitrifiers or denitrifiers. Appl Environ Microbiol44:1342–1348[PubMed]
    [Google Scholar]
  5. Bokranz M., Katz J., Schröder I., Roberton A. M., Kröger A..( 1983;). Energy metabolism and biosynthesis of Vibrio succinogenes growing with nitrate or nitrite as terminal electron acceptor. Arch Microbiol135:36–41 [CrossRef]
    [Google Scholar]
  6. Costa C., Macedo A., Moura I., Moura J. J. G., Le Gall J., Berlier Y., Liu M.-Y., Payne W. J..( 1990;). Regulation of the hexaheme nitrite/nitric oxide reductase of Desulfovibrio desulfuricans, Wolinella succinogenes and Escherichia coli. A mass spectrometric study. FEBS Lett276:67–70 [CrossRef][PubMed]
    [Google Scholar]
  7. Dell’Acqua S., Moura I., Moura J. J. G., Pauleta S. R..( 2011;). The electron transfer complex between nitrous oxide reductase and its electron donors. J Biol Inorg Chem16:1241–1254 [CrossRef][PubMed]
    [Google Scholar]
  8. Einsle O..( 2011;). Structure and function of formate-dependent cytochrome c nitrite reductase, NrfA. Methods Enzymol496:399–422 [CrossRef][PubMed]
    [Google Scholar]
  9. Gilberthorpe N. J., Poole R. K..( 2008;). Nitric oxide homeostasis in Salmonella typhimurium: roles of respiratory nitrate reductase and flavohemoglobin. J Biol Chem283:11146–11154 [CrossRef][PubMed]
    [Google Scholar]
  10. Giles M., Morley N., Baggs E. M., Daniell T. J..( 2012;). Soil nitrate reducing processes - drivers, mechanisms for spatial variation, and significance for nitrous oxide production. Front Microbiol3:407 [CrossRef][PubMed]
    [Google Scholar]
  11. Hartley A. M., Asai R. J..( 1963;). Spectrophotometric determination of nitrate with 2,6-xylenol reagent. Anal Chem35:1207–1213 [CrossRef]
    [Google Scholar]
  12. Heylen K., Keltjens J..( 2012;). Redundancy and modularity in membrane-associated dissimilatory nitrate reduction in Bacillus. Front Microbiol3:371 [CrossRef][PubMed]
    [Google Scholar]
  13. Jones C. M., Graf D. R. H., Bru D., Philippot L., Hallin S..( 2013;). The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J7:417–426 [CrossRef][PubMed]
    [Google Scholar]
  14. Justino M. C., Ecobichon C., Fernandes A. F., Boneca I. G., Saraiva L. M..( 2012;). Helicobacter pylori has an unprecedented nitric oxide detoxifying system. Antioxid Redox Signal17:1190–1200 [CrossRef][PubMed]
    [Google Scholar]
  15. Kaspar H. F., Tiedje J. M..( 1981;). Dissimilatory reduction of nitrate and nitrite in the bovine rumen: nitrous oxide production and effect of acetylene. Appl Environ Microbiol41:705–709[PubMed]
    [Google Scholar]
  16. Kern M., Simon J..( 2009;). Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria. Biochim Biophys Acta1787:646–656 [CrossRef][PubMed]
    [Google Scholar]
  17. Kern M., Eisel F., Scheithauer J., Kranz R. G., Simon J..( 2010;). Substrate specificity of three cytochrome c haem lyase isoenzymes from Wolinella succinogenes: unconventional haem c binding motifs are not sufficient for haem c attachment by NrfI and CcsA1. Mol Microbiol75:122–137 [CrossRef][PubMed]
    [Google Scholar]
  18. Kern M., Klotz M. G., Simon J..( 2011a;). The Wolinella succinogenes mcc gene cluster encodes an unconventional respiratory sulphite reduction system. Mol Microbiol82:1515–1530 [CrossRef][PubMed]
    [Google Scholar]
  19. Kern M., Volz J., Simon J..( 2011b;). The oxidative and nitrosative stress defence network of Wolinella succinogenes: cytochrome c nitrite reductase mediates the stress response to nitrite, nitric oxide, hydroxylamine and hydrogen peroxide. Environ Microbiol13:2478–2494 [CrossRef][PubMed]
    [Google Scholar]
  20. Kröger A., Geisler V., Duchêne A..( 1994;). Isolation of Wolinella succinogenes hydrogenase. Chromatofocusing. A Practical Guide to Membrane Protein Purification141–147 von Jagow G., Schägger H.. London: Academic Press; [CrossRef]
    [Google Scholar]
  21. Kröger A., Biel S., Simon J., Gross R., Unden G., Lancaster C. R. D..( 2002;). Fumarate respiration of Wolinella succinogenes: enzymology, energetics and coupling mechanism. Biochim Biophys Acta1553:23–38 [CrossRef][PubMed]
    [Google Scholar]
  22. Lorenzen J. P., Kröger A., Unden G..( 1993;). Regulation of anaerobic respiratory pathways in Wolinella succinogenes by the presence of electron acceptors. Arch Microbiol159:477–483 [CrossRef]
    [Google Scholar]
  23. Mania D., Heylen K., van Spanning R. J. M., Frostegård Å..( 2014;). The nitrate-ammonifying and nosZ carrying bacterium Bacillus vireti is a potent source and sink for nitric and nitrous oxide under high nitrate conditions. Environ Microbiol [CrossRef][PubMed]
    [Google Scholar]
  24. Molstad L., Dörsch P., Bakken L. R..( 2007;). Robotized incubation system for monitoring gases (O2, NO, N2O N2) in denitrifying cultures. J Microbiol Methods71:202–211 [CrossRef][PubMed]
    [Google Scholar]
  25. Pauleta S. R., Dell’Acqua S., Moura I..( 2013;). Nitrous oxide reductase. Coord Chem Rev257:332–349 [CrossRef]
    [Google Scholar]
  26. Payne W. J., Grant M. A., Shapleigh J., Hoffman P..( 1982;). Nitrogen oxide reduction in Wolinella succinogenes and Campylobacter species. J Bacteriol152:915–918[PubMed]
    [Google Scholar]
  27. Pfennig N., Trüper H. G..( 1981;). Isolation of members of the families Chromatiaceae and Chlorobiaceae. The Prokaryotes279–289 Starr M. P., Stolp H., Trüper H. G., Balous A., Schlegel H. G.. New York, Berlin, Heidelberg: Springer; [CrossRef]
    [Google Scholar]
  28. Pomowski A., Zumft W. G., Kroneck P. M. H., Einsle O..( 2011;). N2O binding at a [4Cu : 2S] copper–sulphur cluster in nitrous oxide reductase. Nature477:234–237 [CrossRef][PubMed]
    [Google Scholar]
  29. Poole R. K..( 2005;). Nitric oxide and nitrosative stress tolerance in bacteria. Biochem Soc Trans33:176–180 [CrossRef][PubMed]
    [Google Scholar]
  30. Reay D. S., Davidson E. A., Smith K. A., Smith P., Melillo J. M., Dentener F., Crutzen P. J..( 2012;). Global agriculture and nitrous oxide emissions. Nature Clim. Change2:410–416 [CrossRef]
    [Google Scholar]
  31. Richardson D. J., Berks B. C., Russell D. A., Spiro S., Taylor C. J..( 2001;). Functional, biochemical and genetic diversity of prokaryotic nitrate reductases. Cell Mol Life Sci58:165–178 [CrossRef][PubMed]
    [Google Scholar]
  32. 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 Biotechnol27:388–397 [CrossRef][PubMed]
    [Google Scholar]
  33. Rider B. F., Mellon M. G..( 1946;). Colorimetric determination of nitrite. Ind Eng Chem18:96–98
    [Google Scholar]
  34. Rowley G., Hensen D., Felgate H., Arkenberg A., Appia-Ayme C., Prior K., Harrington C., Field S. J., Butt J. N..& other authors ( 2012;). Resolving the contributions of the membrane-bound and periplasmic nitrate reductase systems to nitric oxide and nitrous oxide production in Salmonella enterica serovar Typhimurium. Biochem J441:755–762 [CrossRef][PubMed]
    [Google Scholar]
  35. Sambrook J., Fritsch E. F., Maniatis T..( 1989;). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  36. Sanford R. A., Wagner D. D., Wu Q., Chee-Sanford J. C., Thomas S. H., Cruz-García C., Rodríguez G., Massol-Deyá A., Krishnani K. K..& other authors ( 2012;). Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc Natl Acad Sci U S A109:19709–19714 [CrossRef][PubMed]
    [Google Scholar]
  37. Saraiva L. M., Vicente J. B., Teixeira M..( 2004;). The role of the flavodiiron proteins in microbial nitric oxide detoxification. Adv Microb Physiol49:77–129 [CrossRef][PubMed]
    [Google Scholar]
  38. Schumacher W., Kroneck P. M. H..( 1992;). Anaerobic energy metabolism of the sulfur-reducing bacterim “Spirillum“ 5175 during dissimilatory nitrate reduction to ammonia. Arch Microbiol157:464–470 [CrossRef]
    [Google Scholar]
  39. Schumacher W., Kroneck P. M. H., Pfennig N..( 1992;). Comparative systematic study on “Spirillum“ 5175, Campylobacter and Wolinella species. Arch Microbiol158:287–293 [CrossRef]
    [Google Scholar]
  40. Simon J..( 2002;). Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev26:285–309 [CrossRef][PubMed]
    [Google Scholar]
  41. Simon J., Kern M..( 2008;). Quinone-reactive proteins devoid of haem b form widespread membrane-bound electron transport modules in bacterial respiration. Biochem Soc Trans36:1011–1016 [CrossRef][PubMed]
    [Google Scholar]
  42. Simon J., Klotz M. G..( 2013;). Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations. Biochim Biophys Acta1827:114–135 [CrossRef][PubMed]
    [Google Scholar]
  43. Simon J., Kröger A..( 1998;). Identification and characterization of IS1302, a novel insertion element from Wolinella succinogenes belonging to the IS3 family. Arch Microbiol170:43–49 [CrossRef][PubMed]
    [Google Scholar]
  44. Simon J., Kroneck P. M. H..( 2013;). Microbial sulfite respiration. Adv Microb Physiol62:45–117 [CrossRef][PubMed]
    [Google Scholar]
  45. Simon J., Gross R., Ringel M., Schmidt E., Kröger A..( 1998;). Deletion and site-directed mutagenesis of the Wolinella succinogenes fumarate reductase operon. Eur J Biochem251:418–426 [CrossRef][PubMed]
    [Google Scholar]
  46. Simon J., Gross R., Einsle O., Kroneck P. M. H., Kröger A., Klimmek O..( 2000;). A NapC/NirT-type cytochrome c (NrfH) is the mediator between the quinone pool and the cytochrome c nitrite reductase of Wolinella succinogenes. Mol Microbiol35:686–696 [CrossRef][PubMed]
    [Google Scholar]
  47. Simon J., Einsle O., Kroneck P. M. H., Zumft W. G..( 2004;). The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase. FEBS Lett569:7–12 [CrossRef][PubMed]
    [Google Scholar]
  48. Simon J., van Spanning R. J. M., Richardson D. J..( 2008;). The organisation of proton motive and non-proton motive redox loops in prokaryotic respiratory systems. Biochim Biophys Acta1777:1480–1490 [CrossRef][PubMed]
    [Google Scholar]
  49. Simon J., Kern M., Hermann B., Einsle O., Butt J. N..( 2011;). Physiological function and catalytic versatility of bacterial multihaem cytochromes c involved in nitrogen and sulfur cycling. Biochem Soc Trans39:1864–1870 [CrossRef][PubMed]
    [Google Scholar]
  50. Smith K. A..( 2010;). Nitrous Oxide and Climate Change London: Earthscan;
    [Google Scholar]
  51. Stein L. Y..( 2011;). Surveying N2O-producing pathways in bacteria. Methods Enzymol486:131–152 [CrossRef][PubMed]
    [Google Scholar]
  52. Stremińska M. A., Felgate H., Rowley G., Richardson D. J., Baggs E. M..( 2012;). Nitrous oxide production in soil isolates of nitrate-ammonifying bacteria. Environ Microbiol Rep4:66–71 [CrossRef][PubMed]
    [Google Scholar]
  53. Teraguchi S., Hollocher T. C..( 1989;). Purification and some characteristics of a cytochrome c-containing nitrous oxide reductase from Wolinella succinogenes. J Biol Chem264:1972–1979[PubMed]
    [Google Scholar]
  54. Thomson A. J., Giannopoulos G., Pretty J., Baggs E. M., Richardson D. J..( 2012;). Biological sources and sinks of nitrous oxide and strategies to mitigate emissions. Philos Trans R Soc B Biol Sci367:1157–1168 [CrossRef][PubMed]
    [Google Scholar]
  55. van Spanning R. J. M..( 2011;). Structure, function, regulation and evolution of the nitrite and nitrous oxide reductases: denitrification enzymes with a beta-propeller fold. Nitrogen Cycling in Bacteria135–161 Moir J. W. B.. Wymondham: Caister Academic Press;
    [Google Scholar]
  56. Wüst A., Schneider L., Pomowski A., Zumft W. G., Kroneck P. M. H., Einsle O..( 2012;). Nature’s way of handling a greenhouse gas: the copper–sulfur cluster of purple nitrous oxide reductase. Biol Chem393:1067–1077 [CrossRef][PubMed]
    [Google Scholar]
  57. Yoshinari T..( 1980;). N2O reduction by Vibrio succinogenes. Appl Environ Microbiol39:81–84[PubMed]
    [Google Scholar]
  58. Zumft W. G..( 1997;). Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev61:533–616[PubMed]
    [Google Scholar]
  59. Zumft W. G., Kroneck P. M. H..( 2007;). Respiratory transformation of nitrous oxide (N2O) to dinitrogen by Bacteria and Archaea. Adv Microb Physiol52:107–227 [CrossRef][PubMed]
    [Google Scholar]
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