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. 1986 Sep;83(18):6805–6809. doi: 10.1073/pnas.83.18.6805

Anaerobic regulation of nitrogen-fixation genes in Rhodopseudomonas capsulata.

R G Kranz, R Haselkorn
PMCID: PMC386598  PMID: 3018747

Abstract

A Rhodopseudomonas capsulata nifH::lacZ gene fusion was used to isolate constitutive mutants of R. capsulata, unable to repress nif gene transcription anaerobically with every fixed-nitrogen source tested. When these nifc strains were grown aerobically, nif gene transcription was repressed. These results indicate that the regulation of nif gene transcription by fixed nitrogen is different from the regulation by oxygen. Under anaerobic conditions, nif gene transcription in both R. capsulata and Klebsiella pneumoniae is specifically prevented by inhibitors of DNA gyrase [DNA topoisomerase type II (ATP-hydrolyzing), EC 5.99.1.3]. A recent study has shown that anaerobically grown Salmonella typhimurium have high DNA gyrase activity, whereas aerobically grown cells have high DNA topoisomerase type I (EC 5.99.1.2) activity and DNA that is more relaxed [Yamamoto, N. & Droffner, M. L. (1985) Proc. Natl. Acad. Sci. USA 82, 2077-2081]. In view of these results, we suggest that the control of nif gene transcription in response to oxygen is determined by the action of DNA gyrase and DNA topoisomerase I. Thus, although nitrogen control of nif gene expression requires the products of regulatory genes for which constitutive mutations can be isolated, oxygen appears instead to prevent the adoption of a DNA conformation necessary, directly or indirectly, for nif gene transcription.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ausubel F. M. Regulation of nitrogen fixation genes. Cell. 1984 May;37(1):5–6. doi: 10.1016/0092-8674(84)90294-0. [DOI] [PubMed] [Google Scholar]
  2. Avtges P., Kranz R. G., Haselkorn R. Isolation and organization of genes for nitrogen fixation in Rhodopseudomonas capsulata. Mol Gen Genet. 1985;201(3):363–369. doi: 10.1007/BF00331324. [DOI] [PubMed] [Google Scholar]
  3. Avtges P., Scolnik P. A., Haselkorn R. Genetic and physical map of the structural genes (nifH,D,K) coding for the nitrogenase complex of Rhodopseudomonas capsulata. J Bacteriol. 1983 Oct;156(1):251–256. doi: 10.1128/jb.156.1.251-256.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buchanan-Wollaston V., Cannon M. C., Beynon J. L., Cannon F. C. Role of the nifA gene product in the regulation of nif expression in Klebsiella pneumoniae. Nature. 1981 Dec 24;294(5843):776–778. doi: 10.1038/294776a0. [DOI] [PubMed] [Google Scholar]
  5. Burris R. H. Nitrogen fixation--assay methods and techniques. Methods Enzymol. 1972;24:415–431. doi: 10.1016/0076-6879(72)24088-5. [DOI] [PubMed] [Google Scholar]
  6. Cannon M., Hill S., Kavanaugh E., Cannon F. A molecular genetic study of nif expression in Klebsiella pneumoniae at the level of transcription, translation and nitrogenase activity. Mol Gen Genet. 1985;198(2):198–206. doi: 10.1007/BF00382996. [DOI] [PubMed] [Google Scholar]
  7. Collins J. J., Brill W. J. Control of Klebsiella pneumoniae nif mRNA synthesis. J Bacteriol. 1985 Jun;162(3):1186–1190. doi: 10.1128/jb.162.3.1186-1190.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dixon R., Eady R. R., Espin G., Hill S., Iaccarino M., Kahn D., Merrick M. Analysis of regulation of Klebsiella pneumoniae nitrogen fixation (nif) gene cluster with gene fusions. Nature. 1980 Jul 10;286(5769):128–132. doi: 10.1038/286128a0. [DOI] [PubMed] [Google Scholar]
  9. Drlica K. Biology of bacterial deoxyribonucleic acid topoisomerases. Microbiol Rev. 1984 Dec;48(4):273–289. doi: 10.1128/mr.48.4.273-289.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gellert M., O'Dea M. H., Itoh T., Tomizawa J. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4474–4478. doi: 10.1073/pnas.73.12.4474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hallenbeck P. C., Meyer C. M., Vignais P. M. Nitrogenase from the photosynthetic bacterium Rhodopseudomonas capsulata: purification and molecular properties. J Bacteriol. 1982 Feb;149(2):708–717. doi: 10.1128/jb.149.2.708-717.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Han S., Udvardy A., Schedl P. Novobiocin blocks the Drosophila heat shock response. J Mol Biol. 1985 May 5;183(1):13–29. doi: 10.1016/0022-2836(85)90277-3. [DOI] [PubMed] [Google Scholar]
  13. Hill S., Kennedy C., Kavanagh E., Goldberg R. B., Hanau R. Nitrogen fixation gene (nifL) involved in oxygen regulation of nitrogenase synthesis in K. pneumoniae. Nature. 1981 Apr 2;290(5805):424–426. doi: 10.1038/290424a0. [DOI] [PubMed] [Google Scholar]
  14. Kranz R. G., Gennis R. B. Characterization of the cytochrome d terminal oxidase complex of Escherichia coli using polyclonal and monoclonal antibodies. J Biol Chem. 1984 Jun 25;259(12):7998–8003. [PubMed] [Google Scholar]
  15. Kranz R. G., Haselkorn R. Characterization of nif regulatory genes in Rhodopseudomonas capsulata using lac gene fusions. Gene. 1985;40(2-3):203–215. doi: 10.1016/0378-1119(85)90043-5. [DOI] [PubMed] [Google Scholar]
  16. Kubo M., Kano Y., Nakamura H., Nagata A., Imamoto F. In vivo enhancement of general and specific transcription in Escherichia coli by DNA gyrase activity. Gene. 1979 Oct;7(2):153–171. doi: 10.1016/0378-1119(79)90030-1. [DOI] [PubMed] [Google Scholar]
  17. MacNeil D., Zhu J., Brill W. J. Regulation of nitrogen fixation in Klebsiella pneumoniae: isolation and characterization of strains with nif-lac fusions. J Bacteriol. 1981 Jan;145(1):348–357. doi: 10.1128/jb.145.1.348-357.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. MacNeil D., Zhu J., Brill W. J. Regulation of nitrogen fixation in Klebsiella pneumoniae: isolation and characterization of strains with nif-lac fusions. J Bacteriol. 1981 Jan;145(1):348–357. doi: 10.1128/jb.145.1.348-357.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. MacNeil T., Brill W. J., Howe M. M. Bacteriophage mu-induced deletions in a plasmid containing the nif (N2 fixation) genes of Klebsiella pneumoniae. J Bacteriol. 1978 Jun;134(3):821–829. doi: 10.1128/jb.134.3.821-829.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. ORMEROD J. G., ORMEROD K. S., GEST H. Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism. Arch Biochem Biophys. 1961 Sep;94:449–463. doi: 10.1016/0003-9861(61)90073-x. [DOI] [PubMed] [Google Scholar]
  21. Ow D. W., Ausubel F. M. Regulation of nitrogen metabolism genes by nifA gene product in Klebsiella pneumoniae. Nature. 1983 Jan 27;301(5898):307–313. doi: 10.1038/301307a0. [DOI] [PubMed] [Google Scholar]
  22. Sanzey B. Modulation of gene expression by drugs affecting deoxyribonucleic acid gyrase. J Bacteriol. 1979 Apr;138(1):40–47. doi: 10.1128/jb.138.1.40-47.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Smith C. L., Kubo M., Imamoto F. Promoter-specific inhibition of transcription by antibiotics which act on DNA gyrase. Nature. 1978 Oct 5;275(5679):420–423. doi: 10.1038/275420a0. [DOI] [PubMed] [Google Scholar]
  24. Sugino A., Cozzarelli N. R. The intrinsic ATPase of DNA gyrase. J Biol Chem. 1980 Jul 10;255(13):6299–6306. [PubMed] [Google Scholar]
  25. Wall J. D., Braddock K. Mapping of Rhodopseudomonas capsulata nif genes. J Bacteriol. 1984 May;158(2):404–410. doi: 10.1128/jb.158.2.404-410.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Yamamoto N., Droffner M. L. Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2077–2081. doi: 10.1073/pnas.82.7.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yang H. L., Heller K., Gellert M., Zubay G. Differential sensitivity of gene expression in vitro to inhibitors of DNA gyrase. Proc Natl Acad Sci U S A. 1979 Jul;76(7):3304–3308. doi: 10.1073/pnas.76.7.3304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Yen H. C., Marrs B. Map of genes for carotenoid and bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata. J Bacteriol. 1976 May;126(2):619–629. doi: 10.1128/jb.126.2.619-629.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]

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