1887

Abstract

The ability to utilize atmospheric nitrogen (N) as a sole nitrogen source is an important trait for prokaryotes. Knowledge of N fixation by methanotrophs is needed to understand their role in nitrogen cycling in different environments. The verrucomicrobial methanotroph ‘’ strain SolV was investigated for its ability to fix N. Physiological studies were combined with nitrogenase activity measurements and phylogenetic analysis of the genes, encoding the subunits of the nitrogenase. ‘’ SolV was able to fix N at low oxygen (O) concentration (0.5 %, v/v) in chemostat cultures. This low oxygen concentration was also required for an optimal nitrogenase activity [47.4 nmol ethylene h (mg cell dry weight)]. Based on acetylene reduction assay and growth experiments, the nitrogenase of strain SolV seems to be extremely oxygen sensitive compared to most proteobacterial methanotrophs. The activity of the nitrogenase was not inhibited by ammonium concentrations up to 94 mM. This is believed to be the first report on the physiology of N fixation within the phylum .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.036061-0
2010-04-01
2020-07-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/4/1052.html?itemId=/content/journal/micro/10.1099/mic.0.036061-0&mimeType=html&fmt=ahah

References

  1. Auman A. J., Speake C. C., Lidstrom M. E.. 2001; nifH sequences and nitrogen fixation in type I and type II methanotrophs. Appl Environ Microbiol67:4009–4016
    [Google Scholar]
  2. Boetius A., Ravenschlag K., Schubert C. J., Rickert D., Widdel F., Gieseke A., Amann R., Jorgensen B. B., Witte U.. other authors 2000; A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature407:623–626
    [Google Scholar]
  3. Conrad R.. 2009; The global methane cycle: recent advances in understanding the microbial processes involved. Environ Microbiol Reports1:285–292
    [Google Scholar]
  4. Dalton H., Whittenbury R.. 1976; Acetylene reduction technique as an assay for nitrogenase activity in methane oxidizing bacterium Methylococcus capsulatus strain Bath. Arch Microbiol109:147–151
    [Google Scholar]
  5. Davis J. B., Coty V. F., Stanley J. P.. 1964; Atmospheric nitrogen fixation by methane-oxidizing bacteria. J Bacteriol88:468–472
    [Google Scholar]
  6. De Bont J. A. M., Mulder E. G.. 1976; Invalidity of acetylene reduction assay in alkane utilizing, nitrogen-fixing bacteria. Appl Environ Microbiol31:640–647
    [Google Scholar]
  7. Dedysh S. N., Khmelenina V. N., Suzina N. E., Trotsenko Y. A., Semrau J. D., Liesack W., Tiedje J. M.. 2002; Methylocapsa acidiphila gen. nov., sp nov., a novel methane-oxidizing and dinitrogen-fixing acidophilic bacterium from Sphagnum bog. Int J Syst Evol Microbiol52:251–261
    [Google Scholar]
  8. Dedysh S. N., Ricke P., Liesack W.. 2004; NifH and NifD phylogenies: an evolutionary basis for understanding nitrogen fixation capabilities of methanotrophic bacteria. Microbiology150:1301–1313
    [Google Scholar]
  9. Dekas A. E., Poretsky R. S., Orphan V. J.. 2009; Deep-sea Archaea fix and share nitrogen in methane-consuming microbial consortia. Science326:422–426
    [Google Scholar]
  10. Dixon R., Kahn D.. 2004; Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol2:621–631
    [Google Scholar]
  11. Dunfield P. F., Yuryev A., Senin P., Smirnova A. V., Stott M. B., Hou S. B., Ly B., Saw J. H., Zhou Z. M.. other authors 2007; Methane oxidation by an extremely acidophilic bacterium of the phylum Verrucomicrobia. Nature450:879–883
    [Google Scholar]
  12. Ettwig K. F., Shima S., van de Pas-Schoonen K. T., Kahnt J., Medema M. H., Op den Camp H. J. M., Jetten M. S. M., Strous M.. 2008; Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol10:3164–3173
    [Google Scholar]
  13. Felsenstein J.. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution39:783–791
    [Google Scholar]
  14. Hanson R. S., Hanson T. E.. 1996; Methanotrophic bacteria. Microbiol Rev60:439–471
    [Google Scholar]
  15. Hou S. B., Makarova K. S., Saw J. H. W., Senin P., Ly B. V., Zhou Z. M., Ren Y., Wang J. M., Galperin M. Y.. other authors 2008; Complete genome sequence of the extremely acidophilic methanotroph isolate V4, Methylacidiphilum infernorum, a representative of the bacterial phylum Verrucomicrobia. Biol Direct3:26
    [Google Scholar]
  16. Howard J. B., Rees D. C.. 1996; Structural basis of biological nitrogen fixation. Chem Rev96:2965–2982
    [Google Scholar]
  17. Islam T., Jensen S., Reigstad L. J., Larsen O., Birkeland N. K.. 2008; Methane oxidation at 5 °C and pH 2 by a thermoacidophilic bacterium belonging to the Verrucomicrobia phylum. Proc Natl Acad Sci U S A105:300–304
    [Google Scholar]
  18. Mackintosh M. E.. 1978; Nitrogen fixation by Thiobacillus ferrooxidans. J Gen Microbiol105:215–218
    [Google Scholar]
  19. Murrell J. C., Dalton H.. 1983; Nitrogen fixation in obligate methanotrophs. J Gen Microbiol129:3481–3486
    [Google Scholar]
  20. Murrell J. C., Jetten M. S. M.. 2009; The microbial methane cycle. Environ Microbiol Reports1:279–284
    [Google Scholar]
  21. Newton W. E.. 2007; Physiology, biochemistry and molecular biology of nitrogen fixation. In Biology of The Nitrogen Cycle pp109–129 Edited by Bothe H., Ferguson S. J., Newton W. E.. Amsterdam: Elsevier;
  22. Norris P. R., Murrell J. C., Hinson D.. 1995; The potential for diazotrophy in iron-and sulfur-oxidizing acidophilic bacteria. Arch Microbiol164:294–300
    [Google Scholar]
  23. Oakley C. J., Murrell J. C.. 1988; nifH genes in the obligate methane oxidizing bacteria. FEMS Microbiol Lett49:53–57
    [Google Scholar]
  24. Oakley C. J., Murrell J. C.. 1991; Cloning of nitrogenase structural genes from the obligate methanotroph Methylococcus capsulatus (Bath. FEMS Microbiol Lett62:121–126
    [Google Scholar]
  25. Op den Camp H. J. M., Islam T., Stott M. B., Harhangi H. R., Hynes A., Schouten S., Jetten M. S. M., Birkeland N. K., Pol A.. other authors 2009; Environmental, genomic and taxonomic perspectives on methanotrophic Verrucomicrobia. Environ Microbiol Reports1:293–306
    [Google Scholar]
  26. Pol A., Heijmans K., Harhangi H. R., Tedesco D., Jetten M. S. M., Op den Camp H. J. M.. 2007; Methanotrophy below pH 1 by a new Verrucomicrobia species. Nature450:874–879
    [Google Scholar]
  27. Postgate J. R., Eady R. R.. 1988; The evolution of biological nitrogen fixation. In Nitrogen Fixation: Hundred Years After pp31–40 Edited by Bothe H., de Bruijn F. J., Newton W. E.. Stuttgart: Gustav Fischer;
    [Google Scholar]
  28. Raghoebarsing A. A., Pol A., van de Pas-Schoonen K. T., Smolders A. J. P., Ettwig K. F., Rijpstra W. I. C., Schouten S., Damste J. S. S., Op den Camp H. J. M.. other authors 2006; A microbial consortium couples anaerobic methane oxidation to denitrification. Nature440:918–921
    [Google Scholar]
  29. Robson R. L., Postgate J. R.. 1980; Oxygen and hydrogen in biological nitrogen fixation. Annu Rev Microbiol34:183–207
    [Google Scholar]
  30. Rudnick P., Meletzus D., Green A., He L. H., Kennedy C.. 1997; Regulation of nitrogen fixation by ammonium in diazotrophic species of proteobacteria. Soil Biol Biochem29:831–841
    [Google Scholar]
  31. Saitou N., Nei M.. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol4:406–425
    [Google Scholar]
  32. Schönheit P., Brandis A., Thauer R. K.. 1979; Ferredoxin degradation in growing Clostridium pasteurianum during periods of iron deprivation. Arch Microbiol120:73–76
    [Google Scholar]
  33. Takeda K.. 1988; Characteristics of a nitrogen fixing methanotroph, Methylocystis T-1. Antonie Van Leeuwenhoek54:521–534
    [Google Scholar]
  34. Tamura K., Dudley J., Nei M., Kumar S.. 2007; MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol24:1596–1599
    [Google Scholar]
  35. Taylor S., Ninjoor V., Dowd D. M., Tappel A. L.. 1974; Cathepsin B2 measurement by sensitive fluorometric ammonia analysis. Anal Biochem60:153–162
    [Google Scholar]
  36. Toukdarian A. E., Lidstrom M. E.. 1984; Nitrogen metabolism in a new obligate methanotroph, ‘ Methylosinus’ strain 6. J Gen Microbiol130:1827–1837
    [Google Scholar]
  37. Tyson G. W., Lo I., Baker B. J., Allen E. E., Hugenholtz P., Banfield J. F.. 2005; Genome-directed isolation of the key nitrogen fixer Leptospirillum ferrodiazotrophum sp. nov. from an acidophilic microbial community. Appl Environ Microbiol71:6319–6324
    [Google Scholar]
  38. Wagner M., Horn M.. 2006; The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. Curr Opin Biotechnol17:241–249
    [Google Scholar]
  39. Ward N., Larsen O., Sakwa J., Bruseth L., Khouri H., Durkin A. S., Dimitrov G., Jiang L. X., Scanlan D.. other authors 2004; Genomic insights into methanotrophy: the complete genome sequence of Methylococcus capsulatus (Bath. PLoS Biol2:e303
    [Google Scholar]
  40. Young J. P. W.. 1992; Phylogenetic classification of nitrogen-fixing organisms. In Biological Nitrogen Fixation pp43–86 Edited by Stacey G., Evans H. J., Burris R. H. New York: Chapman & Hall;
  41. Zehr J. P., Jenkins B. D., Short S. M., Steward G. F.. 2003; Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol5:539–554
    [Google Scholar]
  42. Zhivotchenko A. G., Nikonova E. S., Jorgensen M. H.. 1995; Effect of fermentation conditions on N2 fixation by Methylococcus capsulatus. Bioprocess Biosyst Eng14:9–15
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.036061-0
Loading
/content/journal/micro/10.1099/mic.0.036061-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error