1887

Abstract

strain 2.4.3, when lacking the oxidase, is unable to transition from aerobic respiration to denitrification using cellular respiration as a means of reducing oxygen levels. This is due to an inability to express , the gene encoding nitrite reductase. Under certain photosynthetic conditions this strain can transition from aerobic to nitrate respiration, demonstrating that expression can occur in the absence of a functional oxidase. If oxygen levels are reduced under non-photosynthetic conditions using low-oxygen gas mixes, nitrite reductase activity is detected at wild-type levels in the strain lacking the oxidase. In addition, co-culture experiments show that incubation of the deficient strain 2.4.3 with 2.4.1, which is deficient but has the high-affinity oxidase, restores denitrification in sealed-vessel experiments. Taken together these results indicate that high end-point O levels are the reason why the strain lacking the oxidase cannot transition from aerobic respiration to denitrification under certain conditions. The protein probably being affected by these O levels is the transcriptional regulator NnrR.

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2010-10-01
2024-04-25
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References

  1. Baek S. H., Hartsock A., Shapleigh J. P. 2008; Agrobacterium tumefaciens C58 uses ActR and FnrN to control nirK and nor expression. J Bacteriol 190:78–86
    [Google Scholar]
  2. Bartnikas T. B., Tosques I. E., Laratta W. P., Shi J., Shapleigh J. P. 1997; Characterization of the nitric oxide reductase-encoding region in Rhodobacter sphaeroides 2.4.3. J Bacteriol 179:3534–3540
    [Google Scholar]
  3. Bedmar E. J., Robles E. F., Delgado M. J. 2005; The complete denitrification pathway of the symbiotic, nitrogen-fixing bacterium Bradyrhizobium japonicum. Biochem Soc Trans 33:141–144
    [Google Scholar]
  4. Chung C. T., Niemela S. L., Miller R. H. 1989; One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solution. Proc Natl Acad Sci U S A 86:2172–2175
    [Google Scholar]
  5. Daldal F., Mandaci S., Winterstein C., Myllykallio H., Duyck K., Zannoni D. 2001; Mobile cytochrome c2 and membrane-anchored cytochrome cY are both efficient electron donors to the cbb3- and aa3-type cytochrome c oxidases during respiratory growth of Rhodobacter sphaeroides. J Bacteriol 183:2013–2024
    [Google Scholar]
  6. de Bruijn F. J., Rossbach S., Bruand C., Parrish J. R. 2006; A highly conserved Sinorhizobium meliloti operon is induced microaerobically via the FixLJ system and by nitric oxide (NO) via NnrR. Environ Microbiol 8:1371–1381
    [Google Scholar]
  7. Eraso J. M., Roh J. H., Zeng X., Callister S. J., Lipton M. S., Kaplan S. 2008; Role of the global transcriptional regulator PrrA in Rhodobacter sphaeroides 2.4.1: combined transcriptome and proteome analysis. J Bacteriol 190:4831–4848
    [Google Scholar]
  8. Forte E., Urbani A., Saraste M., Sarti P., Brunori M., Giuffrè A. 2001; The cytochrome cbb3 from Pseudomonas stutzeri displays nitric oxide reductase activity. Eur J Biochem 268:6486–6491
    [Google Scholar]
  9. Giardina G., Rinaldo S., Johnson K. A., Di Matteo A., Brunori M., Cutruzzola F. 2008; NO sensing in Pseudomonas aeruginosa: structure of the transcriptional regulator DNR. J Mol Biol 378:1002–1015
    [Google Scholar]
  10. Hartsock A., Shapleigh J. P. 2010; Identification, functional studies, and genomic comparisons of new members of the NnrR regulon in Rhodobacter sphaeroides. J Bacteriol 192:903–911
    [Google Scholar]
  11. Hughes M. N. 2008; Chemistry of nitric oxide and related species. Methods Enzymol 436:3–19
    [Google Scholar]
  12. Kovach M. E., Elzer P. H., Hill D. S., Robertson G. T., Farris M. A., Roop R. M. II, Peterson K. M. 1995; Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175–176
    [Google Scholar]
  13. Kwiatkowski A. V., Shapleigh J. P. 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 271:24382–24388
    [Google Scholar]
  14. Kwiatkowski A. V., Laratta W. P., Toffanin A., Shapleigh J. P. 1997; Analysis of the role of the nnrR gene product in the response of Rhodobacter sphaeroides 2.4.1 to exogenous nitric oxide. J Bacteriol 179:5618–5620
    [Google Scholar]
  15. Laratta W. P., Choi P. S., Tosques I. E., Shapleigh J. P. 2002; Involvement of the PrrB/PrrA two-component system in nitrite respiration in Rhodobacter sphaeroides 2.4.3: evidence for transcriptional regulation. J Bacteriol 184:3521–3529
    [Google Scholar]
  16. Laratta W. P., Nanaszko M. J., Shapleigh J. P. 2006; Electron transfer to nitrite reductase of Rhodobacter sphaeroides 2.4.3: examination of cytochromes c2 and cY. Microbiology 152:1479–1488
    [Google Scholar]
  17. Lee Y. Y., Shearer N., Spiro S. 2006; Transcription factor NNR from Paracoccus denitrificans is a sensor of both nitric oxide and oxygen: isolation of nnr* alleles encoding effector-independent proteins and evidence for a haem-based sensing mechanism. Microbiology 152:1461–1470
    [Google Scholar]
  18. Lueking D. R., Fraley R. T., Kaplan S. 1978; Intracytoplasmic membrane synthesis in synchronous cell populations of Rhodopseudomonas sphaeroides. J Biol Chem 253:451–457
    [Google Scholar]
  19. Maniatis T., Fritsch E. F., Sambrook J. 1982 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  20. Morley N., Baggs E. M., Dorsch P., Bakken L. 2008; Production of NO, N2O and N2 by extracted soil bacteria, regulation by and O2 concentrations. FEMS Microbiol Ecol 65:102–112
    [Google Scholar]
  21. O'Gara J. P., Eraso J. M., Kaplan S. 1998; A redox-responsive pathway for aerobic regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 180:4044–4050
    [Google Scholar]
  22. Oh J. I. 2006; Effect of mutations of five conserved histidine residues in the catalytic subunit of the cbb3 cytochrome c oxidase on its function. J Microbiol 44:284–292
    [Google Scholar]
  23. Oh J. I., Ko I. J., Kaplan S. 2004; Reconstitution of the Rhodobacter sphaeroides cbb3-PrrBA signal transduction pathway in vitro. Biochemistry 43:7915–7923
    [Google Scholar]
  24. Pappas C. T., Sram J., Moskvin O. V., Ivanov P. S., Mackenzie R. C., Choudhary M., Land M. L., Larimer F. W., Kaplan S., Gomelsky M. 2004; Construction and validation of the Rhodobacter sphaeroides 2.4.1 DNA microarray: transcriptome flexibility at diverse growth modes. J Bacteriol 186:4748–4758
    [Google Scholar]
  25. Patel R. P., McAndrew J., Sellak H., White C. R., Jo H., Freeman B. A., Darley-Usmar V. 1999; Biological aspects of reactive nitrogen species. Biochim Biophys Acta 1411:385–400
    [Google Scholar]
  26. Preisig O., Zufferey R., Thony-Meyer L., Appleby C. A., Hennecke H. 1996; A high-affinity cbb3-type cytochrome oxidase terminates the symbiosis-specific respiratory chain of Bradyrhizobium japonicum. J Bacteriol 178:1532–1538
    [Google Scholar]
  27. Prentki P., Krisch H. M. 1984; In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313
    [Google Scholar]
  28. Ranson-Olson B., Zeilstra-Ryalls J. 2008; Regulation of the Rhodobacter sphaeroides 2.4.1 hemA gene by PrrA and FnrL. J Bacteriol 190:6769–6778
    [Google Scholar]
  29. Riistama S., Puustinen A., Verkhovsky M. I., Morgan J. E., Wikstrom M. 2000; Binding of O2 and its reduction are both retarded by replacement of valine 279 by isoleucine in cytochrome c oxidase from Paracoccus denitrificans. Biochemistry 39:6365–6372
    [Google Scholar]
  30. Risgaard-Petersen N., Langezaal A. M., Ingvardsen S., Schmid M. C., Jetten M. S., Op C., Derksen J. W., Pina-Ochoa E., Eriksson S. P. other authors 2006; Evidence for complete denitrification in a benthic foraminifer. Nature 443:93–96
    [Google Scholar]
  31. Simon R., Priefer U., Pühler A. 1983; A broad host range mobilization system for in vitro genetic engineering: transposon mutagenesis in gram negative bacteria. Nature Biotechnology 1:784–791
    [Google Scholar]
  32. Spiro S. 2007; Regulators of bacterial responses to nitric oxide. FEMS Microbiol Rev 31:193–211
    [Google Scholar]
  33. Tosques I. E., Shi J., Shapleigh J. P. 1996; Cloning and characterization of nnrR, whose product is required for the expression of proteins involved in nitric oxide metabolism in Rhodobacter sphaeroides 2.4.3. J Bacteriol 178:4958–4964
    [Google Scholar]
  34. Tosques I. E., Kwiatkowski A. V., Shi J., Shapleigh J. P. 1997; Characterization and regulation of the gene encoding nitrite reductase in Rhodobacter sphaeroides 2.4.3. J Bacteriol 179:1090–1095
    [Google Scholar]
  35. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119
    [Google Scholar]
  36. Zumft W. G. 1997; Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev 61:533–616
    [Google Scholar]
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