1887

Abstract

, a photosynthetic diazotroph, is able to regulate nitrogenase activity in response to environmental factors such as ammonium ions or darkness, the so-called switch-off effect. This is due to reversible modification of the Fe-protein, one of the two components of nitrogenase. The signal transduction pathway(s) in this regulatory mechanism is not fully understood, especially not in response to darkness. We have previously shown that the switch-off response and metabolic state differ between cells grown with dinitrogen or glutamate as the nitrogen source, although both represent poor nitrogen sources. In this study we show that pyruvate affects the response to darkness in cultures grown with glutamate as nitrogen source, leading to a response similar to that in cultures grown with dinitrogen. The effects are related to P protein uridylylation and glutamine synthetase activity. We also show that pyruvate induces protein synthesis and that inhibition of pyruvate formate-lyase leads to loss of nitrogenase activity in the dark.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.045831-0
2011-06-01
2020-07-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/6/1834.html?itemId=/content/journal/micro/10.1099/mic.0.045831-0&mimeType=html&fmt=ahah

References

  1. Becker A., Kabsch W..( 2002;). X-ray structure of pyruvate formate-lyase in complex with pyruvate and CoA. How the enzyme uses the Cys-418 thiyl radical for pyruvate cleavage. J Biol Chem277:40036–40042 [CrossRef][PubMed]
    [Google Scholar]
  2. Brush E. J., Lipsett K. A., Kozarich J. W..( 1988;). Inactivation of Escherichia coli pyruvate formate-lyase by hypophosphite: evidence for a rate-limiting phosphorus-hydrogen bond cleavage. Biochemistry27:2217–2222 [CrossRef][PubMed]
    [Google Scholar]
  3. Clark D. P..( 1989;). The fermentation pathways of Escherichia coli. FEMS Microbiol Rev5:223–234 [CrossRef][PubMed]
    [Google Scholar]
  4. Crewther W. G..( 1956;). The inhibition of formic dehydrogenase and formic hydrogenlyase systems of Escherichia coli by hypophosphite. Biochim Biophys Acta21:178–180 [CrossRef][PubMed]
    [Google Scholar]
  5. Dixon R., Kahn D..( 2004;). Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol2:621–631 [CrossRef][PubMed]
    [Google Scholar]
  6. Edgren T., Nordlund S..( 2006;). Two pathways of electron transport to nitrogenase in Rhodospirillum rubrum: the major pathway is dependent on the fix gene products. FEMS Microbiol Lett260:30–35 [CrossRef][PubMed]
    [Google Scholar]
  7. Gest H..( 1951;). Metabolic patterns in photosynthetic bacteria. Bacteriol Rev15:183–210[PubMed]
    [Google Scholar]
  8. Gest H., Kamen M. D..( 1949;). Photoproduction of molecular hydrogen by Rhodospirillum rubrum. Science109:558–559 [CrossRef][PubMed]
    [Google Scholar]
  9. Gorrell T. E., Uffen R. L..( 1977;). Fermentative metabolism of pyruvate by Rhodospirillum rubrum after anaerobic growth in darkness. J Bacteriol131:533–543[PubMed]
    [Google Scholar]
  10. Jonsson A., Nordlund S..( 2007;). In vitro studies of the uridylylation of the three PII protein paralogs from Rhodospirillum rubrum: the transferase activity of R. rubrum GlnD is regulated by α-ketoglutarate and divalent cations but not by glutamine. J Bacteriol189:3471–3478 [CrossRef][PubMed]
    [Google Scholar]
  11. Jonsson A., Teixeira P. F., Nordlund S..( 2007;). The activity of adenylyltransferase in Rhodospirillum rubrum is only affected by α-ketoglutarate and unmodified PII proteins, but not by glutamine, in vitro. FEBS J274:2449–2460 [CrossRef][PubMed]
    [Google Scholar]
  12. Jonsson A., Nordlund S., Teixeira P. F..( 2009;). Reduced activity of glutamine synthetase in Rhodospirillum rubrum mutants lacking the adenylyltransferase GlnE. Res Microbiol160:581–584 [CrossRef][PubMed]
    [Google Scholar]
  13. Jungermann K., Schön G..( 1974;). Pyruvate formate lyase in Rhodospirillum rubrum Ha adapted to anaerobic dark conditions. Arch Microbiol99:109–116 [CrossRef][PubMed]
    [Google Scholar]
  14. Kanemoto R. H., Ludden P. W..( 1984;). Effect of ammonia, darkness, and phenazine methosulfate on whole-cell nitrogenase activity and Fe protein modification in Rhodospirillum rubrum. J Bacteriol158:713–720[PubMed]
    [Google Scholar]
  15. Knappe J., Neugebauer F. A., Blaschkowski H. P., Gänzler M..( 1984;). Post-translational activation introduces a free radical into pyruvate formate-lyase. Proc Natl Acad Sci U S A81:1332–1335 [CrossRef][PubMed]
    [Google Scholar]
  16. Lehtiö L., Leppänen V. M., Kozarich J. W., Goldman A..( 2002;). Structure of Escherichia coli pyruvate formate-lyase with pyruvate. Acta Crystallogr D Biol Crystallogr58:2209–2212 [CrossRef][PubMed]
    [Google Scholar]
  17. Liang J. H., Nielsen G. M., Lies D. P., Burris R. H., Roberts G. P., Ludden P. W..( 1991;). Mutations in the draT and draG genes of Rhodospirillum rubrum result in loss of regulation of nitrogenase by reversible ADP-ribosylation. J Bacteriol173:6903–6909[PubMed]
    [Google Scholar]
  18. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J..( 1951;). Protein measurement with the Folin phenol reagent. J Biol Chem193:265–275[PubMed]
    [Google Scholar]
  19. Ludden P. W., Burris R. H..( 1981;). In vivo and in vitro studies on ATP and electron donors to nitrogenase in Rhodospirillum rubrum. Arch Microbiol130:155–158 [CrossRef]
    [Google Scholar]
  20. Melchiorsen C. R., Jokumsen K. V., Villadsen J., Johnsen M. G., Israelsen H., Arnau J..( 2000;). Synthesis and posttranslational regulation of pyruvate formate-lyase in Lactococcus lactis. J Bacteriol182:4783–4788 [CrossRef][PubMed]
    [Google Scholar]
  21. Merrick M. J., Edwards R. A..( 1995;). Nitrogen control in bacteria. Microbiol Rev59:604–622[PubMed]
    [Google Scholar]
  22. Ninfa A. J., Jiang P..( 2005;). PII signal transduction proteins: sensors of α-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol8:168–173 [CrossRef][PubMed]
    [Google Scholar]
  23. Nordlund S., Ludden P. W..( 2004;). Post-translational regulation of nitrogenase in photosynthetic bacteria. Genetics and Regulation of Nitrogen Fixation in Free-Living Bacteria175–196 Klipp W., Masephol B., Gallon J. R., Newton W. E.. The Netherlands: Kluwer Academic;
    [Google Scholar]
  24. Nordlund S., Kanemoto R. H., Murrell S. A., Ludden P. W..( 1985;). Properties and regulation of glutamine synthetase from Rhodospirillum rubrum. J Bacteriol161:13–17[PubMed]
    [Google Scholar]
  25. Ormerod J. G., Ormerod K. S., Gest H..( 1961;). Light-dependent utilization of organic compounds and photoproduction of molecular hydrogen by photosynthetic bacteria; relationships with nitrogen metabolism. Arch Biochem Biophys94:449–463 [CrossRef][PubMed]
    [Google Scholar]
  26. Rasmussen L. J., Møller P. L., Atlung T..( 1991;). Carbon metabolism regulates expression of the pfl (pyruvate formate-lyase) gene in Escherichia coli. J Bacteriol173:6390–6397[PubMed]
    [Google Scholar]
  27. Rees D. C., Howard J. B..( 2000;). Nitrogenase: standing at the crossroads. Curr Opin Chem Biol4:559–566 [CrossRef][PubMed]
    [Google Scholar]
  28. Sawers G., Suppmann B..( 1992;). Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins. J Bacteriol174:3474–3478[PubMed]
    [Google Scholar]
  29. Teixeira P. F., Jonsson A., Frank M., Wang H., Nordlund S..( 2008;). Interaction of the signal transduction protein GlnJ with the cellular targets AmtB1, GlnE and GlnD in Rhodospirillum rubrum: dependence on manganese, 2-oxoglutarate and the ADP/ATP ratio. Microbiology154:2336–2347 [CrossRef][PubMed]
    [Google Scholar]
  30. Teixeira P. F., Wang H., Nordlund S..( 2010;). Nitrogenase switch-off and regulation of ammonium assimilation in response to light deprivation in Rhodospirillum rubrum are influenced by the nitrogen source used during growth. J Bacteriol192:1463–1466 [CrossRef][PubMed]
    [Google Scholar]
  31. Voelskow H., Schön G..( 1978;). Pyruvate fermentation in light-grown cells of Rhodospirillum rubrum during adaptation to anaerobic dark conditions. Arch Microbiol119:129–133 [CrossRef][PubMed]
    [Google Scholar]
  32. Wang H., Franke C. C., Nordlund S., Norén A..( 2005;). Reversible membrane association of dinitrogenase reductase activating glycohydrolase in the regulation of nitrogenase activity in Rhodospirillum rubrum; dependence on GlnJ and AmtB1. FEMS Microbiol Lett253:273–279 [CrossRef][PubMed]
    [Google Scholar]
  33. Zhang Y., Pohlmann E. L., Ludden P. W., Roberts G. P..( 2001;). Functional characterization of three GlnB homologs in the photosynthetic bacterium Rhodospirillum rubrum: roles in sensing ammonium and energy status. J Bacteriol183:6159–6168 [CrossRef][PubMed]
    [Google Scholar]
  34. Zhang Y., Pohlmann E. L., Roberts G. P..( 2004;). Identification of critical residues in GlnB for its activation of NifA activity in the photosynthetic bacterium Rhodospirillum rubrum. Proc Natl Acad Sci U S A101:2782–2787 [CrossRef][PubMed]
    [Google Scholar]
  35. Zhang Y., Pohlmann E. L., Roberts G. P..( 2005;). GlnD is essential for NifA activation, NtrB/NtrC-regulated gene expression, and posttranslational regulation of nitrogenase activity in the photosynthetic, nitrogen-fixing bacterium Rhodospirillum rubrum. J Bacteriol187:1254–1265 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.045831-0
Loading
/content/journal/micro/10.1099/mic.0.045831-0
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