Skip to content
1887

Microbiology Society logo Microbiology

Volume 161, Issue 11

Phosphoribulokinase mediates nitrogenase-induced carbon dioxide fixation gene repression in Open Access

Abstract

In many organisms there is a balance between carbon and nitrogen metabolism. These observations extend to the nitrogen-fixing, nonsulfur purple bacteria, which have the classic family of P(II) regulators that coordinate signals of carbon and nitrogen status to regulate nitrogen metabolism. Curiously, these organisms also possess a reverse mechanism to regulate carbon metabolism based on cellular nitrogen status. In this work, studies in firmly established that the activity of the enzyme that catalyses nitrogen fixation, nitrogenase, induces a signal that leads to repression of genes encoding enzymes of the Calvin–Benson–Bassham (CBB) CO fixation pathway. Additionally, genetic and metabolomic experiments revealed that NADH-activated phosphoribulokinase is an intermediate in the signalling pathway. Thus, nitrogenase activity appears to be linked to gene repression through phosphoribulokinase.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000160
2015-11-01
2025-05-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/11/2184.html?itemId=/content/journal/micro/10.1099/mic.0.000160&mimeType=html&fmt=ahah

References

  1. Biegel E., Schmidt S., González J.M., Müller V. (2011). Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotesCell Mol Life Sci 68613–634 [View Article][PubMed]. [Google Scholar]
  2. Dangel A.W., Tabita F.R. (2009). Protein-protein interactions between CbbR and RegA (PrrA), transcriptional regulators of the cbb operons of Rhodobacter sphaeroidesMol Microbiol 71717–729 [View Article][PubMed]. [Google Scholar]
  3. Dangel A.W., Gibson J.L., Janssen A.P., Tabita F.R. (2005). Residues that influence in vivo and in vitro CbbR function in Rhodobacter sphaeroides and identification of a specific region critical for co-inducer recognitionMol Microbiol 571397–1414 [View Article][PubMed]. [Google Scholar]
  4. Dixon R., Kahn D. (2004). Genetic regulation of biological nitrogen fixationNat Rev Microbiol 2621–631 [View Article][PubMed]. [Google Scholar]
  5. Doucette C.D., Schwab D.J., Wingreen N.S., Rabinowitz J.D. (2011). α-Ketoglutarate coordinates carbon and nitrogen utilization via enzyme I inhibitionNat Chem Biol 7894–901 [View Article][PubMed]. [Google Scholar]
  6. Dubbs J.M., Tabita F.R. (1998). Two functionally distinct regions upstream of the cbbI operon of Rhodobacter sphaeroides regulate gene expressionJ Bacteriol 1804903–4911[PubMed]. [Google Scholar]
  7. Dubbs J.M., Tabita F.R. (2003). Interactions of the cbbII promoter-operator region with CbbR and RegA (PrrA) regulators indicate distinct mechanisms to control expression of the two cbb operons of Rhodobacter sphaeroidesJ Biol Chem 27816443–16450 [View Article][PubMed]. [Google Scholar]
  8. Dubbs J.M., Tabita F.R. (2004). Regulators of nonsulfur purple phototrophic bacteria and the interactive control of CO2 assimilation, nitrogen fixation, hydrogen metabolism and energy generationFEMS Microbiol Rev 28353–376 [View Article][PubMed]. [Google Scholar]
  9. Dubbs J.M., Bird T.H., Bauer C.E., Tabita F.R. (2000). Interaction of CbbR and RegA* transcription regulators with the Rhodobacter sphaeroides cbbI Promoter-operator regionJ Biol Chem 27519224–19230 [View Article][PubMed]. [Google Scholar]
  10. Edgren T., Nordlund S. (2004). The fixABCX genes in Rhodospirillum rubrum encode a putative membrane complex participating in electron transfer to nitrogenaseJ Bacteriol 1862052–2060 [View Article][PubMed]. [Google Scholar]
  11. Farmer R.M., Laguna R., Panescu J., McCoy A., Logsdon B., Zianni M., Moskvin O.V., Gomelsky M., Tabita F.R. (2014). Altered residues in key proteins influence the expression and activity of the nitrogenase complex in an adaptive CO2 fixation-deficient mutant strain of Rhodobacter sphaeroidesMicrobiology 160198–208 [View Article][PubMed]. [Google Scholar]
  12. Forchhammer K. (2007). Glutamine signalling in bacteriaFront Biosci 12358–370 [View Article][PubMed]. [Google Scholar]
  13. Gibson J.L., Tabita F.R. (1987). Organization of phosphoribulokinase and ribulose bisphosphate carboxylase/oxygenase genes in Rhodopseudomonas (Rhodobacter) sphaeroidesJ Bacteriol 1693685–3690[PubMed]. [Google Scholar]
  14. Gibson J.L., Tabita F.R. (1993). Nucleotide sequence and functional analysis of cbbR, a positive regulator of the Calvin cycle operons of Rhodobacter sphaeroidesJ Bacteriol 1755778–5784[PubMed]. [Google Scholar]
  15. Gibson J.L., Dubbs J.M., Tabita F.R. (2002). Differential expression of the CO2 fixation operons of Rhodobacter sphaeroides by the Prr/Reg two-component system during chemoautotrophic growthJ Bacteriol 1846654–6664 [View Article][PubMed]. [Google Scholar]
  16. Haaker H., de Kok A., Veeger C. (1974). Regulation of dinitrogen fixation in intact Azotobacter vinelandiiBiochim Biophys Acta 357344–357 [View Article][PubMed]. [Google Scholar]
  17. Hillmer P., Gest H. (1977). H2 metabolism in the photosynthetic bacterium Rhodopseudomonas capsulata: production and utilization of H2 by resting cellsJ Bacteriol 129732–739[PubMed]. [Google Scholar]
  18. Hoffman B.M., Lukoyanov D., Dean D.R., Seefeldt L.C. (2013). Nitrogenase: a draft mechanismAcc Chem Res 46587–595 [View Article][PubMed]. [Google Scholar]
  19. Joshi H.M., Tabita F.R. (1996). A global two component signal transduction system that integrates the control of photosynthesis, carbon dioxide assimilation, and nitrogen fixationProc Natl Acad Sci U S A 9314515–14520 [View Article][PubMed]. [Google Scholar]
  20. Joshi G.S., Zianni M., Bobst C.E., Tabita F.R. (2012). Further unraveling the regulatory twist by elucidating metabolic coinducer-mediated CbbR-cbbI promoter interactions in Rhodopseudomonas palustris CGA010J Bacteriol 1941350–1360 [View Article][PubMed]. [Google Scholar]
  21. Jouanneau Y., Tabita F.R. (1986). Independent regulation of synthesis of form I and form II ribulose bisphosphate carboxylase-oxygenase in Rhodopseudomonas sphaeroidesJ Bacteriol 165620–624[PubMed]. [Google Scholar]
  22. Kobayashi D., Tamoi M., Iwaki T., Shigeoka S., Wadano A. (2003). Molecular characterization and redox regulation of phosphoribulokinase from the cyanobacterium Synechococcus sp. PCC 7942Plant Cell Physiol 44269–276 [View Article][PubMed]. [Google Scholar]
  23. Laguna R., Tabita F.R., Alber B.E. (2011). Acetate-dependent photoheterotrophic growth and the differential requirement for the Calvin-Benson-Bassham reductive pentose phosphate cycle in Rhodobacter sphaeroides and Rhodopseudomonas palustrisArch Microbiol 193151–154 [View Article][PubMed]. [Google Scholar]
  24. Ludden P.W. (1991). Energetics of and sources of energy for biological nitrogen fixation. In Current Topics in Bioenergetics, pp. 369–390vol. 16. San Diego, CAAcademic Press [View Article]. [Google Scholar]
  25. Masepohl B., Kranz R.G. (2009). Regulation of nitrogen fixation. In The Purple Phototrophic Bacteria23rd edn., pp. 759–775. Edited by Hunter C. N., Daldal F., Thurnauer M. C., Beatty J. T.DordrechtSpringer [View Article]. [Google Scholar]
  26. McEwan A.G. (1994). Photosynthetic electron transport and anaerobic metabolism in purple non-sulfur phototrophic bacteriaAntonie van Leeuwenhoek 66151–164 [View Article][PubMed]. [Google Scholar]
  27. McKinlay J.B., Harwood C.S. (2010). Carbon dioxide fixation as a central redox cofactor recycling mechanism in bacteriaProc Natl Acad Sci U S A 10711669–11675 [View Article][PubMed]. [Google Scholar]
  28. Miziorko H.M. (2000). Phosphoribulokinase: current perspectives on the structure/function basis for regulation and catalysisAdv Enzymol Relat Areas Mol Biol 7495–127[PubMed]. [Google Scholar]
  29. Ninfa A.J. (2007). Regulation of carbon and nitrogen metabolism: adding regulation of ion channels and another second messenger to the mixProc Natl Acad Sci U S A 1044243–4244 [View Article][PubMed]. [Google Scholar]
  30. Nordlund S., Hoglund L. (1986). Studies of the adenylate and pyridine nucleotide pools during nitrogenase ‘switch-off’ in Rhodospirillum rubrumPlant Soil 90203–209 [View Article]. [Google Scholar]
  31. Norén A., Nordlund S. (1994). Changes in the NAD(P)H concentration caused by addition of nitrogenase ‘switch-off’ effectors in Rhodospirillum rubrum G-9, as measured by fluorescenceFEBS Lett 35643–45 [View Article][PubMed]. [Google Scholar]
  32. Novak J.S., Tabita F.R. (1999). Molecular approaches to probe differential NADH activation of phosphoribulokinase isozymes from Rhodobacter sphaeroidesArch Biochem Biophys 363273–282 [View Article][PubMed]. [Google Scholar]
  33. Paschen A., Drepper T., Masepohl B., Klipp W. (2001). Rhodobacter capsulatus nifA mutants mediating nif gene expression in the presence of ammoniumFEMS Microbiol Lett 200207–213 [View Article][PubMed]. [Google Scholar]
  34. Rey F.E., Heiniger E.K., Harwood C.S. (2007). Redirection of metabolism for biological hydrogen productionAppl Environ Microbiol 731665–1671 [View Article][PubMed]. [Google Scholar]
  35. Rindt K.P., Ohmann E. (1969). NADH and AMP as allosteric effectors of ribulose-5-phosphate kinase in Rhodopseudomonas spheroidesBiochem Biophys Res Commun 36357–364 [View Article][PubMed]. [Google Scholar]
  36. Schell M.A. (1993). Molecular biology of the LysR family of transcriptional regulatorsAnnu Rev Microbiol 47597–626 [View Article][PubMed]. [Google Scholar]
  37. Schneider K., Asao M., Carter M.S., Alber B.E. (2012). Rhodobacter sphaeroides uses a reductive route via propionyl coenzyme A to assimilate 3-hydroxypropionateJ Bacteriol 194225–232 [View Article][PubMed]. [Google Scholar]
  38. Selao T.T., Nordlund S., Norén A. (2008). Comparative proteomic studies in Rhodospirillum rubrum grown under different nitrogen conditionsJ Proteome Res 73267–3275 [View Article][PubMed]. [Google Scholar]
  39. Simon R., Priefer U., Pühler A. (1983). A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in Gram negative bacteriaNat Biotechnol 1784–791 [View Article]. [Google Scholar]
  40. Smith S.A., Tabita F.R. (2002). Up-regulated expression of the cbb(I) and cbb(II) operons during photoheterotrophic growth of a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion mutant of Rhodobacter sphaeroidesJ Bacteriol 1846721–6724 [View Article][PubMed]. [Google Scholar]
  41. Tabita F.R. (1988). Molecular and cellular regulation of autotrophic carbon dioxide fixation in microorganismsMicrobiol Rev 52155–189[PubMed]. [Google Scholar]
  42. Tabita F.R. (1995). The biochemistry and metabolic regulation of carbon metabolism and CO2 fixation in purple bacteria. In Anoxygenic Photosynthetic Bacteria. Edited by Blankenship R. E., Madigan M. T., Bauer C. E.DordrechtKluwer Academic Publishers. [Google Scholar]
  43. Tamoi M., Murakami A., Takeda T., Shigeoka S. (1998). Lack of light/dark regulation of enzymes involved in the photosynthetic carbon reduction cycle in cyanobacteria, Synechococcus PCC 7942 and Synechocystis PCC 6803Biosci Biotechnol Biochem 62374–376 [View Article]. [Google Scholar]
  44. Tamoi M., Miyazaki T., Fukamizo T., Shigeoka S. (2005). The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditionsPlant J 42504–513 [View Article][PubMed]. [Google Scholar]
  45. Tao Y., Liu D., Yan X., Zhou Z., Lee J.K., Yang C. (2012). Network identification and flux quantification of glucose metabolism in Rhodobacter sphaeroides under photoheterotrophic H(2)-producing conditionsJ Bacteriol 194274–283 [View Article][PubMed]. [Google Scholar]
  46. Tichi M.A., Tabita F.R. (2000). Maintenance and control of redox poise in Rhodobacter capsulatus strains deficient in the Calvin-Benson-Bassham pathwayArch Microbiol 174322–333 [View Article][PubMed]. [Google Scholar]
  47. Tichi M.A., Tabita F.R. (2001). Interactive control of Rhodobacter capsulatus redox-balancing systems during phototrophic metabolismJ Bacteriol 1836344–6354 [View Article][PubMed]. [Google Scholar]
  48. van Niel C.B. (1944). The culture, general physiology, morphology, and classification of the non-sulfur purple and brown bacteriaBacteriol Rev 81–118[PubMed]. [Google Scholar]
  49. VerBerkmoes N.C., Shah M.B., Lankford P.K., Pelletier D.A., Strader M.B., Tabb D.L., McDonald W.H., Barton J.W., Hurst G.B., other authors. (2006). Determination and comparison of the baseline proteomes of the versatile microbe Rhodopseudomonas palustris under its major metabolic statesJ Proteome Res 5287–298 [View Article][PubMed]. [Google Scholar]
  50. Wang D., Zhang Y., Pohlmann E.L., Li J., Roberts G.P. (2011). The poor growth of Rhodospirillum rubrum mutants lacking RubisCO is due to the accumulation of ribulose-1,5-bisphosphateJ Bacteriol 1933293–3303 [View Article][PubMed]. [Google Scholar]
  51. Wu J., Bauer C.E. (2008). RegB/RegA, a global redox-responding two-component systemAdv Exp Med Biol 631131–148 [View Article][PubMed]. [Google Scholar]
  52. Wu J., Bauer C.E. (2010). RegB kinase activity is controlled in part by monitoring the ratio of oxidized to reduced ubiquinones in the ubiquinone poolMBio 1e00272–e10 [View Article][PubMed]. [Google Scholar]
  53. Yanisch-Perron C., Vieira J., Messing J. (1985). Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectorsGene 33103–119 [View Article][PubMed]. [Google Scholar]
/content/journal/micro/10.1099/mic.0.000160
Loading
Phosphoribulokinase mediates nitrogenase-induced carbon dioxide fixation gene repression in Rhodobacter sphaeroides
Microbiology 161, 2184 (2015); https://doi.org/10.1099/mic.0.000160
/content/journal/micro/10.1099/mic.0.000160
/content/journal/micro/10.1099/mic.0.000160
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited 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