1887

Abstract

MH-110 possesses three different sets of genes for ribulose 1,5-bisphosphate carboxylase/oxygenase (RubisCO): two form I ( and ) and one form II (). We have previously shown that the expression of these RubisCO genes is dependent on the ambient CO concentration. LysR-type transcriptional regulators, designated CbbR1 and CbbRm, are encoded upstream of the and genes, respectively. In this study, we revealed by gel shift assay that CbbR1 and CbbRm bind with higher affinity to the promoter regions of and , respectively, and with lower affinity to the other RubisCO gene promoters. The expression patterns of the three RubisCOs in the and the gene mutants showed that CbbR1 and CbbRm were required to activate the expression of and , respectively, and that neither CbbR1 nor CbbRm was required for the expression of . The expression of was significantly enhanced under high-CO conditions in the mutant, in which the expression of was decreased. Although was not expressed under high-CO conditions in the wild-type strain or the single mutants, the expression of was observed in the double mutant, in which the expression of both and was decreased. These results indicate that there is an interactive regulation among the three RubisCO genes.

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2005-11-01
2020-04-07
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References

  1. Ashida H., Saito Y., Kojima C., Kobayashi K., Ogasawara N., Yokota A. 2003; A functional link between RuBisCO-like protein of Bacillus and photosynthetic RuBisCO. Science302:286–290[CrossRef]
    [Google Scholar]
  2. Badger M. R., Price G. D. 2003; CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot54:609–622[CrossRef]
    [Google Scholar]
  3. Blondelet-Rouault M. H., Weiser J., Lebrihi A., Branny P., Pernodet J. L. 1997; Antibiotic resistance gene cassettes derived from the Ω interposon for use in E. coli and Streptomyces . Gene190:315–317[CrossRef]
    [Google Scholar]
  4. Cannon G. C., Baker S. H., Soyer F.. 7 other authors 2003; Organization of carboxysome genes in the thiobacilli. Curr Microbiol46:115–119[CrossRef]
    [Google Scholar]
  5. Chung S. Y., Yaguchi T., Nishihara H., Igarashi Y., Kodama T. 1993; Purification of form L2 RubisCO from a marine obligately autotrophic hydrogen-oxidizing bacterium, Hydrogenovibrio marinus strain MH-110. FEMS Microbiol Lett109:49–53[CrossRef]
    [Google Scholar]
  6. Dubbs J. M., Tabita F. R. 2003; Interactions of the cbb II promoter-operator region with CbbR and RegA (PrrA) regulators indicate distinct mechanisms to control expression of the two cbb operons of Rhodobacter sphaeroides . J Biol Chem278:16443–16450[CrossRef]
    [Google Scholar]
  7. Dubbs J. M., Bird T. H., Bauer C. E., Tabita F. R. 2000; Interaction of CbbR and RegA* transcription regulators with the Rhodobacter sphaeroides cbb I promoter-operator region. J Biol Chem275:19224–19230[CrossRef]
    [Google Scholar]
  8. Dubbs P., Dubbs J. M., Tabita F. R. 2004; Effector-mediated interaction of CbbRI and CbbRII regulators with target sequences in Rhodobacter capsulatus . J Bacteriol186:8026–8035[CrossRef]
    [Google Scholar]
  9. Falcone D. L., Tabita F. R. 1993; Complementation analysis and regulation of CO2 fixation gene expression in a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion strain of Rhodospirillum rubrum . J Bacteriol175:5066–5077
    [Google Scholar]
  10. Figurski D. H., Helinski D. R. 1979; Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A76:1648–1652[CrossRef]
    [Google Scholar]
  11. Finn M. W., Tabita F. R. 2003; Synthesis of catalytically active form III ribulose 1,5-bisphosphate carboxylase/oxygenase in archaea. J Bacteriol185:3049–3059[CrossRef]
    [Google Scholar]
  12. Gibson J. L., Tabita F. R. 1993; Nucleotide sequence and functional analysis of cbbR , a positive regulator of the Calvin cycle operons of Rhodobacter sphaeroides . J Bacteriol175:5778–5784
    [Google Scholar]
  13. Gibson J. L., Falcone D. L., Tabita F. R. 1991; Nucleotide sequence, transcriptional analysis, and expression of genes encoded within the form I CO2 fixation operon of Rhodobacter sphaeroides . J Biol Chem266:14646–14653
    [Google Scholar]
  14. Grzeszik C., Jeffke T., Schäferjohann J., Kusian B., Bowien B. 2000; Phosphoenolpyruvate is a signal metabolite in transcriptional control of the cbb CO2 fixation operons in Ralstonia eutropha . J Mol Microbiol Biotechnol2:311–320
    [Google Scholar]
  15. Hallenbeck P. L., Lerchen R., Hessler P., Kaplan S. 1990a; Phosphoribulokinase activity and regulation of CO2 fixation critical for photosynthetic growth of Rhodobacter sphaeroides . J Bacteriol172:1749–1761
    [Google Scholar]
  16. Hallenbeck P. L., Lerchen R., Hessler P., Kaplan S. 1990b; Roles of CfxA, CfxB, and external electron acceptors in regulation of ribulose 1,5-bisphosphate carboxylase/oxygenase expression in Rhodobacter sphaeroides . J Bacteriol172:1736–1748
    [Google Scholar]
  17. Hanson T. E., Tabita F. R. 2001; A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc Natl Acad Sci U S A98:4397–4402[CrossRef]
    [Google Scholar]
  18. Hayashi N. R., Oguni A., Yaguchi T., Chung S. Y., Nishihara H., Kodama T., Igarashi Y. 1998; Different properties of gene products of three sets of ribulose 1,5-bisphosphate carboxylase/oxygenase from a marine obligately autotrophic hydrogen-oxidizing bacterium, Hydrogenovibrio marinus strain MH-110. J Ferment Bioeng85:150–155[CrossRef]
    [Google Scholar]
  19. Jouanneau Y., Tabita F. R. 1986; Independent regulation of synthesis of form I and form II ribulose bisphosphate carboxylase-oxygenase in Rhodopseudomonas sphaeroides . J Bacteriol165:620–624
    [Google Scholar]
  20. Kitano K., Maeda N., Fukui T., Atomi H., Imanaka T., Miki K. 2001; Crystal structure of a novel-type archaeal rubisco with pentagonal symmetry. Structure9:473–481[CrossRef]
    [Google Scholar]
  21. Kusano T., Sugawara K. 1993; Specific binding of Thiobacillus ferrooxidan s RbcR to the intergenic sequence between the rbc operon and the rbcR gene. J Bacteriol175:1019–1025
    [Google Scholar]
  22. Kusian B., Bowien B. 1995; Operator binding of the CbbR protein, which activates the duplicate cbb CO2 assimilation operons of Alcaligenes eutrophus . J Bacteriol177:6568–6574
    [Google Scholar]
  23. Kusian B., Bowien B. 1997; Organization and regulation of cbb CO2 assimilation genes in autotrophic bacteria. FEMS Microbiol Rev21:135–155[CrossRef]
    [Google Scholar]
  24. Meijer W. G., van den Bergh E. R. E., Smith L. M. 1996; Induction of the gap-pgk operon encoding glyceraldehyde-3-phosphate dehydrogenase and 3-phosphoglycerate kinase of Xanthobacter flavus requires the LysR-type transcriptional activator CbbR. J Bacteriol178:881–887
    [Google Scholar]
  25. Nishihara H., Igarashi Y., Kodama T. 1989; Isolation of an obligately chemolithoautotrophic, halophilic and aerobic hydrogen-oxidizing bacterium from marine environment. Arch Microbiol152:39–43[CrossRef]
    [Google Scholar]
  26. Nishihara H., Igarashi Y., Kodama T. 1991; Hydrogenovibrio marinus gen. nov., sp. nov., a marine obligately chemolithoautotrophic hydrogen-oxidizing bacterium. Int J Syst Bacteriol41:130–133[CrossRef]
    [Google Scholar]
  27. Paoli G. C., Vichivanives P., Tabita F. R. 1998; Physiological control and regulation of the Rhodobacter capsulatus cbb operons. J Bacteriol180:4258–4269
    [Google Scholar]
  28. Parales R. E., Harwood C. S. 1993; Construction and use of a new broad-host-range lacZ transcriptional fusion vector, pHRP309, for Gram bacteria. Gene133:23–30[CrossRef]
    [Google Scholar]
  29. Penfold R. J., Pemberton J. M. 1992; An improved suicide vector for construction of chromosomal insertion mutations in bacteria. Gene118:145–146[CrossRef]
    [Google Scholar]
  30. Sambrook J., Fritsch E. F., Maniatis T. 1989; Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  31. Sarles L. S., Tabita F. R. 1983; Derepression of the synthesis of d-ribulose 1,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum . J Bacteriol153:458–464
    [Google Scholar]
  32. Schell M. A. 1993; Molecular biology of the LysR family of transcriptional regulators. Annu Rev Microbiol47:597–626[CrossRef]
    [Google Scholar]
  33. Simon R., Priefer U. B, Pühler A. 1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology1:784–791[CrossRef]
    [Google Scholar]
  34. Smith S. A., Tabita F. R. 2002; Up-regulated expression of the cbb I and c bb II operons during photoheterotrophic growth of a ribulose 1,5-bisphosphate carboxylase-oxygenase deletion mutant of Rhodobacter sphaeroides . J Bacteriol184:6721–6724[CrossRef]
    [Google Scholar]
  35. Terazono K., Hayashi N. R., Igarashi Y. 2001; CbbR, a LysR-type transcriptional regulator from Hydrogenophilus thermoluteolus , binds two cbb promoter regions. FEMS Microbiol Lett198:151–157[CrossRef]
    [Google Scholar]
  36. Tichi M. A., Tabita F. R. 2002; Metabolic signals that lead to control of CBB gene expression in Rhodobacter capsulatus . J Bacteriol184:1905–1915[CrossRef]
    [Google Scholar]
  37. van den Bergh E. R. E., Dijkhuizen L., Meijer W. G. 1993; CbbR, a LysR-type transcriptional activator, is required for expression of the autotrophic CO2 fixation enzymes of Xanthobacter flavus . J Bacteriol175:6097–6104
    [Google Scholar]
  38. van Keulen G., Girbal L., van den Bergh E. R. E., Dijkhuizen L., Meijer W. G. 1998; The LysR-type transcriptional regulator CbbR controlling autotrophic CO2 fixation by Xanthobacter flavus is an NADPH sensor. J Bacteriol180:1411–1417
    [Google Scholar]
  39. van Keulen G., Ridder A. N., Dijkhuizen L., Meijer W. G. 2003; Analysis of DNA binding and transcriptional activation by the LysR-type transcriptional regulator CbbR of Xanthobacter flavus . J Bacteriol185:1245–1252[CrossRef]
    [Google Scholar]
  40. Vichivanives P., Bird T. H., Bauer C. E., Tabita F. R. 2000; Multiple regulators and their interactions in vivo and in vitro with the cbb regulons of Rhodobacter capsulatus . J Mol Biol300:1079–1099[CrossRef]
    [Google Scholar]
  41. Windhövel U., Bowien B. 1991; Identification of cfxR , an activator gene of autotrophic CO2 fixation in Alcaligenes eutrophus . Mol Microbiol5:2695–2705[CrossRef]
    [Google Scholar]
  42. Yaguchi T., Chung S. Y., Igarashi Y., Kodama T. 1994; Cloning and sequence of the L2 form of RubisCO from a marine obligately autotrophic hydrogen-oxidizing bacterium, Hydrogenovibrio marinus strain MH-110. Biosci Biotechnol Biochem58:1733–1737[CrossRef]
    [Google Scholar]
  43. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene33:103–119[CrossRef]
    [Google Scholar]
  44. Yoshizawa Y., Toyoda K., Arai H., Ishii M., Igarashi Y. 2004; CO2-responsive expression and gene organization of three ribulose-1,5-bisphosphate carboxylase/oxygenase enzymes and carboxysomes in Hydrogenovibrio marinus strain MH-110. J Bacteriol186:5685–5691[CrossRef]
    [Google Scholar]
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