The nitrate-ammonifying and nosZ-carrying bacterium Bacillus vireti is a potent source and sink for nitric and nitrous oxide under high nitrate conditions

Environmental Microbiology

Volumn 16, Issue 10, 2014, Pages 3196-3210

  Mania, Daniel ^a   Heylen, Kim ^b   van Spanning, Rob J M ^c   Frostegård, Åsa ^a  

^a NORWEGIAN UNIVERSITY OF LIFE SCIENCES   (Norway)

^b GHENT UNIVERSITY   (Belgium)

^c VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS VIRETI; BACTERIA (MICROORGANISMS);

AMMONIUM DERIVATIVE; NITRIC ACID DERIVATIVE; NITRIC OXIDE; NITRITE; NITROGEN; NITROUS OXIDE; OXIDOREDUCTASE;

BACILLUS; BACTERIAL GENOME; DENITRIFICATION; GENETICS; METABOLISM; MOLECULAR GENETICS;

AMMONIUM COMPOUNDS; BACILLUS; DENITRIFICATION; GENOME, BACTERIAL; MOLECULAR SEQUENCE DATA; NITRATES; NITRIC OXIDE; NITRITES; NITROGEN; NITROUS OXIDE; OXIDOREDUCTASES;

EID: 84907877119     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12478     Document Type: Article

References (70)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
2. Arkenberg, A., Runkel, S., Richardson, D.J., and Rowley, G. (2011) The production and detoxification of a potent cytotoxin, nitric oxide, by pathogenic enteric bacteria. Biochem Soc Trans 39: 1876-1879.
3. Aziz, R.K., Bartels, D., Best, A.A., DeJongh, M., Disz, T., Edwards, R.A., etal. (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9: 75.
4. Bakken, L.R., Bergaust, L., Liu, B., and Frostegård, Å. (2012) Regulation of denitrification at the cellular level: a clue to the understanding of N2O emissions from soils. Philos Trans R Soc Lond B Biol Sci 367: 1226-1234.
5. Bendtsen, J.D., Jensen, L.J., Blom, N., Von Heijne, G., and Brunak, S. (2004) Feature-based prediction of non-classical and leaderless protein secretion. Protein Eng Des Sel 17: 349-356.
6. Bendtsen, J.D., Nielsen, H., Widdick, D., Palmer, T., and Brunak, S. (2005) Prediction of twin-arginine signal peptides. BMC Bioinformatics 6: 167.
7. Bergaust, L., Shapleigh, J., Frostegård, Å., and Bakken, L. (2008) Transcription and activities of NOx reductases in Agrobacterium tumefaciens: the influence of nitrate, nitrite and oxygen availability. Environ Microbiol 10: 3070-3081.
8. Bergaust, L., Mao, Y., Bakken, L.R., and Frostegård, Å. (2010) Denitrification response patterns during the transition to anoxic respiration and posttranscriptional effects of suboptimal pH on nitrous [corrected] oxide reductase in Paracoccus denitrificans. Appl Environ Microbiol 76: 6387-6396.
9. Bleakley, B.H., and Tiedje, J.M. (1982) Nitrous oxide production by organisms other than nitrifiers or denitrifiers. Appl Environ Microbiol 44: 1342-1348.
10. Bokranz, M., Katz, J., Schröder, I., Roberton, A.M., and Kröger, A. (1983) Energy metabolism and biosynthesis of Vibrio succinogenes growing with nitrate or nitrite as terminal electron acceptor. Arch Microbiol 135: 36-41.
11. Bonin, P. (1996) Anaerobic nitrate reduction to ammonium in two strains isolated from coastal marine sediment: a dissimilatory pathway. FEMS Microbiol Ecol 19: 27-38.
12. Borodovsky, M., and McIninch, J. (1993) GENMARK: parallel gene recognition for both DNA strands. Comput Chem 17: 123-133.
13. Burgin, A.J., and Hamilton, S.K. (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5: 89-96.
14. Clarke, T.A., Mills, P.C., Poock, S.R., Butt, J.N., Cheesman, M.R., Cole, J.A., etal. (2008) Escherichia coli cytochrome c nitrite reductase NrfA. Methods Enzymol 437: 63-77.
15. Cole, J. (1996) Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol Lett 136: 1-11.
16. Cole, J., and Brown, C. (1980) Nitrite reduction to ammonia by fermentative bacteria: a short circuit in the biological nitrogen cycle. FEMS Microbiol Lett 7: 65-72.
17. Coleman, K.J., Cornish-Bowden, A., and Cole, J.A. (1978) Purification and properties of nitrite reductase from Escherichia coli K12. Biochem J 175: 483-493.
18. Cox, R.D. (1980) Determination of nitrate and nitrite at the parts per billion level by chemiluminescence. Anal Chem 52: 332-335.
19. Cruz Ramos, H., Hoffmann, T., Marino, M., Nedjari, H., Presecan-Siedel, E., Dreesen, O., etal. (2000) Fermentative metabolism of Bacillus subtilis: physiology and regulation of gene expression. J Bacteriol 182: 3072-3080.
20. Darwin, A., Tormay, P., Page, L., Griffiths, L., and Cole, J. (1993) Identification of the formate dehydrogenases and genetic determinants of formate-dependent nitrite reduction by Escherichia coli K12. J Gen Microbiol 139: 1829-1840.
21. Dechorgnat, J., Nguyen, C.T., Armengaud, P., Jossier, M., Diatloff, E., Filleur, S., and Daniel-Vedele, F. (2011) From the soil to the seeds: the long journey of nitrate in plants. J Exp Bot 62: 1349-1359.
22. Einsle, O., Messerschmidt, A., Stach, P., Bourenkov, G.P., Bartunik, H.D., Huber, R., and Kroneck, P.M. (1999) Structure of cytochrome c nitrite reductase. Nature 400: 476-480.
23. Einsle, O., Messerschmidt, A., Huber, R., Kroneck, P.M., and Neese, F. (2002) Mechanism of the six-electron reduction of nitrite to ammonia by cytochrome c nitrite reductase. J Am Chem Soc 124: 11737-11745.
24. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971.
25. Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution (N. Y) 39: 783-791.
26. Felske, A., Wolterink, A., Van Lis, R., and Akkermans, A.D.L. (1998) Phylogeny of the main bacterial 16S rRNA sequences in Drentse A grassland soils (The Netherlands). Appl Environ Microbiol 64: 871-879.
27. Griess, P. (1879) Bemerkungen zu der Abhandlung der HH. Weselsky und Benedikt 'Ueber einige Azoverbindungen'. Berichte der Dtsch Chem Gesellschaft 12: 426-428.
28. Hausladen, A., Gow, A., and Stamler, J.S. (2001) Flavohemoglobin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen. Proc Natl Acad Sci USA 98: 10108-10112.
29. Hemp, J., and Gennis, R.B. (2008) Diversity of the heme-copper superfamily in Archaea: insights from genomics and structural modeling. Results Probl Cell Differ 45: 1-31.
30. Heylen, K., and Keltjens, J. (2012) Redundancy and modularity in membrane-associated dissimilatory nitrate reduction in Bacillus. Front Microbiol 3: 371.
31. Heyndrickx, M., Vauterin, L., Vandamme, P., Kersters, K., and De Vos, P. (1996) Applicability of combined amplified ribosomal DNA restriction analysis (ARDRA) patterns in bacterial phylogeny and taxonomy. J Microbiol Methods 26: 247-259.
32. Heyrman, J., Vanparys, B., Logan, N.A., Balcaen, A., Rodríguez-Díaz, M., Felske, A., and De Vos, P. (2004) Bacillus novalis sp. nov., Bacillus vireti sp. nov., Bacillus soli sp. nov., Bacillus bataviensis sp. nov. and Bacillus drentensis sp. nov., from the Drentse A grasslands. Int J Syst Evol Microbiol 54: 47-57.
33. Käll, L., Krogh, A., and Sonnhammer, E.L.L. (2004) A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338: 1027-1036.
34. Kelso, B., Smith, R.V., Laughlin, R.J., and Lennox, S.D. (1997) Dissimilatory nitrate reduction in anaerobic sediments leading to river nitrite accumulation. Appl Environ Microbiol 63: 4679-4685.
35. Kern, M., and Simon, J. (2009) Electron transport chains and bioenergetics of respiratory nitrogen metabolism in Wolinella succinogenes and other Epsilonproteobacteria. Biochim Biophys Acta 1787: 646-656.
36. Kim, S.O., Orii, Y., Lloyd, D., Hughes, M.N., and Poole, R.K. (1999) Anoxic function for the Escherichia coli flavohaemoglobin (Hmp): reversible binding of nitric oxide and reduction to nitrous oxide. FEBS Lett 445: 389-394.
37. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
38. Lukashin, A.V., and Borodovsky, M. (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26: 1107-1115.
39. MacArthur, P.H., Shiva, S., and Gladwin, M.T. (2007) Measurement of circulating nitrite and S-nitrosothiols by reductive chemiluminescence. J Chromatogr B 851: 93-105.
40. Marino, M., Hoffmann, T., Schmid, R., Möbitz, H., and Jahn, D. (2000) Changes in protein synthesis during the adaptation of Bacillus subtilis to anaerobic growth conditions. Microbiology 146: 97-105.
41. Marsili, R.T., Ostapenko, H., Simmons, R.E., and Green, D.E. (1981) High performance liquid chromatographic determination of organic acids in dairy products. J Food Sci 46: 52-57.
42. Molstad, L., Dörsch, P., and Bakken, L.R. (2007) Robotized incubation system for monitoring gases (O2, NO, N2O N2) in denitrifying cultures. J Microbiol Methods 71: 202-211.
43. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A.C., and Kanehisa, M. (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35: 182-185.
44. Narvhus, J.A., Osteraas, K., Mutukumira, T., and Abrahamsen, R.K. (1998) Production of fermented milk using a malty compound-producing strain of Lactococcus lactis subsp. lactis biovar. diacetylactis, isolated from Zimbabwean naturally fermented milk. Int J Food Microbiol 41: 73-80.
45. Nei, M., and Kumar, S. (2000) Molecular Evolution and Phylogenetics. New York, USA: Oxford University Press.
46. Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
47. Pitcher, D.G., Saunders, N.A., and Owen, R.J. (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8: 151-156.
48. Poole, R.K. (2005) Nitric oxide and nitrosative stress tolerance in bacteria. Biochem Soc Trans 33: 176-180.
49. Rahman, O., Cummings, S.P., Harrington, D.J., and Sutcliffe, I.C. (2008) Methods for the bioinformatic identification of bacterial lipoproteins encoded in the genomes of Gram-positive bacteria. World J Microbiol Biotechnol 24: 2377-2382.
50. Rowley, G., Hensen, D., Felgate, H., Arkenberg, A., Appia-Ayme, C., Prior, K., etal. (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 J 441: 755-762.
51. Rütting, T., Boeckx, P., Müller, C., and Klemedtsson, L. (2011) Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences 8: 1779-1791.
52. Salzberg, S.L., Delcher, A.L., Kasif, S., and White, O. (1998) Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26: 544-548.
53. Schnorpfeil, M., Janausch, I.G., Biel, S., Kröger, A., and Unden, G. (2001) Generation of a proton potential by succinate dehydrogenase of Bacillus subtilis functioning as a fumarate reductase. Eur J Biochem 268: 3069-3074.
54. Silver, W.L., Herman, D.J., and Firestone, M.K. (2001) Dissimilatory nitrate reduction to ammonium in upland tropical forest soils. Ecology 82: 2410-2416.
55. Simon, J. (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26: 285-309.
56. Simon, J., Einsle, O., Kroneck, P.M.H., and 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 Lett 569: 7-12.
57. Stremińska, M.A., Felgate, H., Rowley, G., Richardson, D.J., and Baggs, E.M. (2012) Nitrous oxide production in soil isolates of nitrate-ammonifying bacteria. Environ Microbiol Rep 4: 66-71.
58. Strohm, T.O., Griffin, B., Zumft, W.G., and Schink, B. (2007) Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73: 1420-1424.
59. Suharti, and de Vries, S. (2005) Membrane-bound denitrification in the Gram-positive bacterium Bacillus azotoformans. Biochem Soc Trans 33: 130-133.
60. Suharti, Strampraad, M.J., Schröder, I., and de Vries, S. (2001) A novel copper A containing menaquinol NO reductase from Bacillus azotoformans. Biochemistry 40: 2632-2639.
61. Suharti, Heering, H.A., and de Vries, S. (2004) NO reductase from Bacillus azotoformans is a bifunctional enzyme accepting electrons from menaquinol and a specific endogenous membrane-bound cytochrome c551. Biochemistry 43: 13487-13495.
62. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
63. Tiedje, J.M., Sexstone, A.J., Myrold, D.D., and Robinson, J.A. (1982) Denitrification: ecological niches, competition and survival. Antonie Van Leeuwenhoek 48: 569-583.
64. Verbaendert, I., Boon, N., De Vos, P., and Heylen, K. (2011) Denitrification is a common feature among members of the genus Bacillus. Syst Appl Microbiol 34: 385-391.
65. Vermeiren, J., Van de Wiele, T., Verstraete, W., Boeckx, P., and Boon, N. (2009) Nitric oxide production by the human intestinal microbiota by dissimilatory nitrate reduction to ammonium. J Biomed Biotechnol 2009: 1-10.
66. Vine, C.E., and Cole, J.A. (2011) Unresolved sources, sinks, and pathways for the recovery of enteric bacteria from nitrosative stress. FEMS Microbiol Lett 325: 99-107.
67. de Vries, W., Niekus, H.G.D., Boellaard, M., and Stouthamer, A.H. (1980) Growth yields and energy generation by Campylobacter sputorum subspecies bubulus during growth in continuous culture with different hydrogen acceptors. Arch Microbiol 124: 221-227.
68. Wang, H., and Gunsalus, R.P. (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.
69. Willis, R.B., Montgomery, M.E., and Allen, P.R. (1996) Improved method for manual, colorimetric determination of total Kjeldahl nitrogen using salicylate. J Agric Food Chem 44: 1804-1807.
70. Zdobnov, E.M., and Apweiler, R. (2001) InterProScan - an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.