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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26090-0
2003-04-01
2021-10-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/4/mic149941.html?itemId=/content/journal/micro/10.1099/mic.0.26090-0&mimeType=html&fmt=ahah

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 Microbiol 142:403–408
    [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 Bacteriol 181:2802–2806
    [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 Lett 265:85–87
    [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 Acta 1232:97–173
    [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 J 309:983–992
    [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 Microbiol 44:245–255
    [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 Microbiol 33:341–346
    [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 J 175:483–493
    [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 Bacteriol 180:4192–4198
    [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 Microbiology 40:645–650
    [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 Bacteriol 184:4767–4774
    [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 Lett 177:263–270
    [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 Bacteriol 184:1693–1702
    [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 Microbiol 19:467–481
    [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 Acta 1017:209–216
    [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 Biochem 63:530–536
    [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 Lett 150:277–280
    [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 Microbiol 136:300–305
    [Google Scholar]
  19. McEwan A. G., Jackson J. B., Ferguson S. J. 1984; Rationalisation of properties of nitrate reductases in Rhodopseudomonas capsulata . Arch Microbiol 137:344–349
    [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 Bacteriol 164:823–830
    [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 Microbiol 147:340–345
    [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 J 344:77–84
    [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 Physiol 45:51–112
    [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 Microbiol 19:1307–1318
    [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 J 331:897–904
    [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 Microbiol 157:535–537
    [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 Microbiol 150:131–137
    [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 Biochem 194:263–270
    [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 Sci 58:165–178
    [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 Microbiol 29:241–245
    [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. Microbiology 143:3767–3774
    [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. Microbiology 146:2977–2985
    [Google Scholar]
  33. Shultz J. E., Weaver P. F. 1982; Fermentation and anaerobic respiration by Rhodospirillum rubrum and Rhodopseudomonas capsulata . J Bacteriol 149:181–190
    [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 Bacteriol 175:5867–5876
    [Google Scholar]
  35. Taylor M. A., Jackson J. B. 1985; Threshold dependence of bacterial growth on the protonmotive force. FEBS Lett 192:199–203
    [Google Scholar]
  36. Weaver P. F., Hall J. D., Gest H. 1975; Characterisation of Rhodopseudomonas capsulata . Arch Microbiol 105:207–216
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.26090-0
Loading
/content/journal/micro/10.1099/mic.0.26090-0
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