1887

Abstract

N22DNAR possesses a periplasmic nitrate reductase and is capable of reducing nitrate to nitrite under anaerobic conditions. In the absence of light this ability cannot support chemoheterotrophic growth in batch cultures. This study investigated the effect of nitrate reduction on the growth of N22DNAR during multiple light–dark cycles of anaerobic photoheterotrophic/dark chemoheterotrophic growth conditions in carbon-limited continuous cultures. The reduction of nitrate did not affect the photoheterotrophic growth yield of N22DNAR. After a transition from photoheterotrophic to dark chemoheterotrophic growth conditions, the reduction of nitrate slowed the initial washout of a N22DNAR culture. Towards the end of a period of darkness nitrate-reducing cultures maintained higher viable cell counts than non-nitrate-reducing cultures. During light–dark cycling of a mixed culture, the strain able to reduce nitrate (N22DNAR) outcompeted the strain which was unable to reduce nitrate (N22). The evidence indicates that the periplasmic nitrate reductase activity supports slow growth that retards the washout of a culture during anaerobic chemoheterotrophic conditions, and provides a protonmotive force for cell maintenance during the dark period before reillumination. This translates into a selective advantage during repeated light–dark cycles, such that in mixed culture N22DNAR outcompetes N22. Exposure to light–dark cycles will be a common feature for in its natural habitats, and this study shows that nitrate respiration may provide a selective advantage under such conditions.

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2003-04-01
2020-01-23
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References

  1. Alef K., Jackson J. B., McEwan A. G., Ferguson S. J.. 1984; The activities of two pathways of nitrate respiration in Rhodopseudomonas capsulata . Arch Microbiol142:403–408
    [Google Scholar]
  2. Bedzyk L., Wang T., Ye R. E.. 1999; The periplasmic nitrate reductase in Pseudomonas sp. strain G-179 catalyses the first step of denitrification. J Bacteriol181:2802–2806
    [Google Scholar]
  3. Bell L. C., Richardson D. J., Ferguson S. J.. 1990; Periplasmic and membrane-bound respiratory nitrate reductases in Thiospheara pantotropha . The periplasmic enzyme catalyses the first step in aerobic denitrification. FEBS Lett265:85–87
    [Google Scholar]
  4. Berks B. C., Ferguson S. J., Moir J. W., Richardson D. J.. 1995a; Enzymes and electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochim Biophys Acta1232:97–173
    [Google Scholar]
  5. Berks B. C., Richardson D. J., Reilly A., Willis A. C., Ferguson S. J.. 1995b; The napEDABC gene cluster encoding the periplasmic nitrate reductase system of Thiosphaera pantotropha . Biochem J309:983–992
    [Google Scholar]
  6. Brondijk T. H., Fiegen D., Richardson D. J., Cole J. A.. 2002; Roles of NapF, NapG and NapH, subunits of the Escherichia coli periplasmic nitrate reductase, in ubiquinol oxidation. Mol Microbiol44:245–255
    [Google Scholar]
  7. Castillo F., Dobao M. M., Reyes F., Blasco R., Roldan M. D., Gavira M., Caballero F. J., Moreno V. C., Martinez-Luque M.. 1996; Molecular and regulatory properties of the nitrate reducing systems of Rhodobacter. Curr Microbiol33:341–346
    [Google Scholar]
  8. Coleman K. J., Cornish-Bowden A., Cole J. A.. 1978; Purification and properties of nitrite reductase from Escherichia coli K-12. Biochem J175:483–493
    [Google Scholar]
  9. Darwin A. J., Ziegelhoffer E. C., Kiley P. J., Stewart V.. 1998; Fnr, NarP and NarL regulation of Escherichia coli K-12 napF (periplasmic nitrate reductase) operon transcription in vitro . J Bacteriol180:4192–4198
    [Google Scholar]
  10. Dobao M. M., Martinez-Luque M., Moreno V. C., Castillo F.. 1994; Effect of carbon and nitrogen metabolism on nitrate reductase activity of Rhodobacter capsulatus E1F1. Can J Microbiology40:645–650
    [Google Scholar]
  11. Ellington M. J. K., Bhakoo K. K., Sawers G., Richardson D. J., Ferguson S. J.. 2002; Hierarchy of carbon source selection in Paracoccus pantotrophus : strict correlation between reduction state of the carbon substrate and aerobic expression of the nap operon. J Bacteriol184:4767–4774
    [Google Scholar]
  12. Flanagan D. A., Gregory L. G., Carter J. P., Karakas-Sen A., Richardson D. J., Spiro S.. 1999; Detection of genes for periplasmic nitrate reductase in nitrate respiring bacteria and in community DNA. FEMS Microbiology Lett177:263–270
    [Google Scholar]
  13. Gavira M., Roldan M. D., Castillo F., Moreno-Vivian C.. 2002; Regulation of nap gene expression and periplasmic nitrate reductase activity in the phototrophic bacterium Rhodobacter sphaeroides DSM158. J Bacteriol184:1693–1702
    [Google Scholar]
  14. Grove J., Tanapongpipat S., Thomas G., Griffiths L., Crooke H., Cole J.. 1996; Escherichia coli K-12 genes essential for the synthesis of c -type cytochromes and a third nitrate reductase located in the periplasm. Mol Microbiol19:467–481
    [Google Scholar]
  15. Jones M. R., Richardson D. J., McEwan A. G., Jackson J. B., Ferguson S. J.. 1990; In vivo redox poising of the cyclic electron transport system of Rhodobacter capsulatus and the effects of auxiliary oxidants nitrate, nitrous oxide and trimetylamine N -oxide as revealed by multiple short flash excitation. Biochim Biophys Acta1017:209–216
    [Google Scholar]
  16. Liu H. P., Takio S., Satoh T., Yamamoto I.. 1999; Involvement in denitrification of the napKEFDABC genes encoding the periplasmic nitrate reductase system in the denitrifying phototrophic bacterium Rhodobacter sphaeroides f.sp. denitrificans . Biosci Biotechnol Biochem63:530–536
    [Google Scholar]
  17. McEwan A. G., George C. L., Ferguson S. J., Jackson J. B.. 1982; A nitrate reductase activity in Rhodopseudomonas capsulata linked to electron transfer and generation of a membrane potential. FEBS Lett150:277–280
    [Google Scholar]
  18. McEwan A. G., Ferguson S. J., Jackson J. B.. 1983; Electron flow to dimethylsulphoxide or trimethylamine- N -oxide generates a membrane potential in Rhodopseudomonas capsulata . Arch Microbiol136:300–305
    [Google Scholar]
  19. McEwan A. G., Jackson J. B., Ferguson S. J.. 1984; Rationalisation of properties of nitrate reductases in Rhodopseudomonas capsulata . Arch Microbiol137:344–349
    [Google Scholar]
  20. McEwan A. G., Greenfield A. J., Wetzstein H. G., Jackson J. B., Ferguson S. J.. 1985; Nitrous oxide reduction by members of the family Rhodospirillaceae and nitrous oxide reductase of Rhodopseudomonas capsulata . J Bacteriol164:823–830
    [Google Scholar]
  21. McEwan A. G., Wetzstein H. G., Meyer O., Jackson J. B., Ferguson S. J.. 1987; The periplasmic nitrate reductase of Rhodobacter capsulatus : purification, characterisation and distinction from a single reductase for trimethylamine- N -oxide, dimethylsulfoxide and chlorate. Arch Microbiol147:340–345
    [Google Scholar]
  22. Potter L. C., Millington P., Griffiths L., Thomas G. H., Cole J. A.. 1999; Competition between Escherichia coli strains expressing either a periplasmic or a membrane-bound nitrate reductase: does Nap confer a selective advantage during nitrate limited growth?. Biochem J344:77–84
    [Google Scholar]
  23. Potter L. C., Angove H., Richardson D. J., Cole J.. 2001; Nitrate reduction in the periplasm of gram-negative bacteria. Adv Microb Physiol45:51–112
    [Google Scholar]
  24. Reyes F., Roldan M. D., Klipp W., Castillo F., Moreno-Vivian C.. 1996; Isolation of periplasmic nitrate reductase genes from Rhodobacter sphaeroides DSM158: structural and functional differences among prokaryotic nitrate reductases. Mol Microbiol19:1307–1318
    [Google Scholar]
  25. Reyes F., Gavira M., Castillo F., Moreno-Vivian C.. 1998; Periplasmic nitrate-reducing system of the phototrophic bacterium Rhodobacter sphaeroides DSM 158: transcriptional and mutational analysis of the napKEFDABC gene cluster. Biochem J331:897–904
    [Google Scholar]
  26. Richardson D. J., Ferguson S. J.. 1992; The influence of carbon substrate on the activity of the periplasmic nitrate reductase in aerobically grown Thiosphaera pantotropha . Arch Microbiol157:535–537
    [Google Scholar]
  27. Richardson D. J., King G. F., Kelly D. J., McEwan A. G., Ferguson S. J., Jackson J. B.. 1988; The role of auxiliary oxidants in maintaining cellular redox balance during phototrophic growth of Rhodobacter capsulatus on propionate and butyrate. Arch Microbiol150:131–137
    [Google Scholar]
  28. Richardson D. J., McEwan A. G., Page M. D., Jackson J. B., Ferguson S. J.. 1990; The identification of cytochromes involved in the transfer of electrons to the periplasmic reductase of Rhodobacter capsulatus and resolution of a soluble nitrate reductase–cytochrome c 552 redox complex. Eur J Biochem194:263–270
    [Google Scholar]
  29. 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
    [Google Scholar]
  30. Roldan M. D., Reyes F., Moreno-Vivian C., Castillo F.. 1994; Chlorate and nitrate reduction in the phototrophic bacteria Rhodobacter capsulatus and Rhodobacter sphaeroides . Curr Microbiol29:241–245
    [Google Scholar]
  31. Sears H. J., Spiro S., Richardson D. J.. 1997; Effect of carbon substrate and aeration on nitrate reduction and expression of the periplasmic and membrane bound nitrate reductases in carbon-limited cultures of Paracoccus denitrificans Pd1222. Microbiology143:3767–3774
    [Google Scholar]
  32. Sears H. J., Sawers G., Berks B. C., Ferguson S. J., Richardson D. J.. 2000; Control of periplasmic nitrate reductase gene expression ( napEDABC) from Paracoccus pantotrophus in response to oxygen and carbon substrates. Microbiology146:2977–2985
    [Google Scholar]
  33. Shultz J. E., Weaver P. F.. 1982; Fermentation and anaerobic respiration by Rhodospirillum rubrum and Rhodopseudomonas capsulata . J Bacteriol149:181–190
    [Google Scholar]
  34. Siddiqui R. A., Warnecke-Eberz U., Hengsberger A., Schneider B., Kostka S., Friedrich B.. 1993; Structure and function of a periplasmic nitrate reductase in Alcaligenes eutrophus H16. J Bacteriol175:5867–5876
    [Google Scholar]
  35. Taylor M. A., Jackson J. B.. 1985; Threshold dependence of bacterial growth on the protonmotive force. FEBS Lett192:199–203
    [Google Scholar]
  36. Weaver P. F., Hall J. D., Gest H.. 1975; Characterisation of Rhodopseudomonas capsulata . Arch Microbiol105:207–216
    [Google Scholar]
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