1887

Abstract

A regulatory protein, PpaA, involved in photosystem formation in the anoxygenic phototrophic proteobacterium has been identified and characterized . Based on the phenotypes of cells expressing the gene in extra copy and on the phenotype of the null mutant, it was concluded that PpaA activates photopigment production and operon expression under aerobic conditions. This is in contrast to the function of the PpaA homologue from , AerR, which acts as a repressor under aerobic conditions [ Dong, C., Elsen, S., Swem, L. R. & Bauer, C. E. (2002) . 184, 2805–2814]. The expression of the gene increases several-fold in response to a decrease in oxygen tension, suggesting that the PpaA protein is active under conditions of low or no oxygen. However, no discernible phenotype of a null mutant was observed under anaerobic conditions tested thus far. The photosystem gene repressor PpsR mediates repression of gene expression under aerobic conditions. Sequence analysis of PpaA homologues from several anoxygenic phototrophic bacteria revealed a putative corrinoid-binding domain. It is suggested that PpaA binds a corrinoid cofactor and the availability or structure of this cofactor affects PpaA activity.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.25972-0
2003-02-01
2024-12-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/149/2/mic149377.html?itemId=/content/journal/micro/10.1099/mic.0.25972-0&mimeType=html&fmt=ahah

References

  1. Abada E. M, Balzer A, Jäger A., Klug G. 2002; Bacteriochlorophyll-dependent expression of genes for pigment-binding proteins in Rhodobacter capsulatus involves the RegB/RegA two-component system. Mol Genet Genet 267:202–209
    [Google Scholar]
  2. Altschul S. F, Madden T. L, Schaffer A. A, Zhang J, Zhang Z, Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402
    [Google Scholar]
  3. Amaratunga M, Fluhr K, Jarrett J. T, Drennan C. L, Ludwig M. L, Matthews R. G., Scholten J. D. 1996; A synthetic module for the metH gene permits facile mutagenesis of the cobalamin-binding region of Escherichia coli methionine synthase: initial characterization of seven mutant proteins. Biochemistry 35:2453–2463
    [Google Scholar]
  4. Beinert H., Kiley P. J. 1999; Fe–S proteins in sensing and regulatory functions. Curr Opin Chem Biol 3:152–157
    [Google Scholar]
  5. Braatsch S, Gomelsky M, Kuphal S., Klug G. 2002; A single flavoprotein, AppA, integrates both redox and light signals in Rhodobacter sphaeroides . Mol Microbiol 45:827–836
    [Google Scholar]
  6. Cervantes M., Murillo F. J. 2002; Role of vitamin B12 in light induction of gene expression in the bacterium Myxococcus xanthus . J Bacteriol 184:2215–2224
    [Google Scholar]
  7. Choudhary M., Kaplan S. 2000; DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2.4.1. Nucleic Acids Res 28:862–867
    [Google Scholar]
  8. Christie J. M., Briggs W. R. 2001; Blue light sensing in higher plants. J Biol Chem 276:11457–11460 erratum 17620
    [Google Scholar]
  9. Cohen-Bazire G, Sistrom W. R., Stanier R. Y. 1957; Kinetic studies of pigment synthesis by non-sulfur bacteria. J Cell Comp Physiol 49:25–68
    [Google Scholar]
  10. Comolli J. C, Carl A. J, Hall C., Donohue T. 2002; Transcriptional activation of the Rhodobacter sphaeroides cytochrome c 2 gene P2 promoter by the response regulator PrrA. J Bacteriol 184:390–399
    [Google Scholar]
  11. Dong C, Elsen S, Swem L. R., Bauer C. E. 2002; AerR, a second aerobic repressor of photosynthesis gene expression in Rhodobacter capsulatus . J Bacteriol 184:2805–2814
    [Google Scholar]
  12. Drennan C. L, Huang S, Drummond J. T, Matthews R. G., Ludwig M. L. 1994; How a protein binds B12: A 3·0 Å X-ray structure of B12-binding domains of methionine synthase. Science 266:1669–1674
    [Google Scholar]
  13. Dryden S. C., Kaplan S. 1990; Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides . Nucleic Acids Res 18:7267–7277
    [Google Scholar]
  14. Eraso J. M., Kaplan S. 1994; prrA , a putative response regulator involved in oxygen regulation of photosynthesis gene expression in Rhodobacter sphaeroides . J Bacteriol 176:32–43
    [Google Scholar]
  15. Eraso J. M., Kaplan S. 1995; Oxygen-insensitive synthesis of the photosynthetic membranes of Rhodobacter sphaeroides : a mutant histidine kinase. J Bacteriol 177:2695–2706
    [Google Scholar]
  16. Gilles-Gonzalez M. A. 2001; Oxygen signal transduction. Life 51:165–173
    [Google Scholar]
  17. Gomelsky M., Kaplan S. 1994; Identification of transcriptional factors involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. In Abstracts of the VIII International Symposium on Phototrophic Prokaryotes, abstract 41B. Sant'Angelo in Vado Italy: Tipografia Grafica Valdese;
    [Google Scholar]
  18. Gomelsky M., Kaplan S. 1995a; Genetic evidence that PpsR from Rhodobacter sphaeroides 2.4.1 functions as a repressor of puc and bchF expression. J Bacteriol 177:1634–1637
    [Google Scholar]
  19. Gomelsky M., Kaplan S. 1995b; Isolation of regulatory mutants in photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1 and partial complementation of a PrrB mutant by the HupT histidine-kinase. Microbiology 141:1805–1819
    [Google Scholar]
  20. Gomelsky M., Kaplan S. 1995c; appA , a novel gene encoding a trans -acting factor involved in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 177:4609–4618
    [Google Scholar]
  21. Gomelsky M., Kaplan S. 1997; Molecular genetic analysis suggesting interactions between AppA and PpsR in the regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J Bacteriol 179:128–134
    [Google Scholar]
  22. Gomelsky M., Kaplan S. 1998; AppA, a redox regulator of photosystem formation in Rhodobacter sphaeroides 2.4.1, is a flavoprotein. Identification of a novel FAD binding domain. J Biol Chem 273:35319–35325
    [Google Scholar]
  23. Gomelsky M., Klug G. 2002; BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem Sci 27:497–500
    [Google Scholar]
  24. Gomelsky M, Horne I. M, Lee H. J, Pemberton J. M, McEwan A. G., Kaplan S. 2000; Domain structure, oligomeric state, and mutational analysis of PpsR, the Rhodobacter sphaeroides repressor of photosystem gene expression. J Bacteriol 182:2253–2261
    [Google Scholar]
  25. Gough S. P, Petersen B. O., Duus J. O. 2000; Anaerobic chlorophyll isocyclic ring formation in Rhodobacter capsulatus requires a cobalamin cofactor. Proc Natl Acad Sci U S A 97:6908–6913
    [Google Scholar]
  26. Gregor J., Klug G. 1999; Regulation of bacterial photosynthesis genes by oxygen and light. FEMS Microbiol Lett 179:1–9
    [Google Scholar]
  27. Horne I. M, Pemberton J. M., McEwan A. G. 1996; Photosynthesis gene expression in Rhodobacter sphaeroides is regulated by redox changes which are linked to electron transport. Microbiology 142:2831–2838
    [Google Scholar]
  28. Horne I. M, Williams T. A, Smith D. J, Pemberton J. M., McEwan A. G. 1997; The role of the ppa - ppsR locus in the regulation of photosynthetic gene expression in Rhodobacter sphaeroides . In Abstracts of the IX International Symposium on Phototrophic Prokaryotes Vienna, Austria: , abstract 100B
    [Google Scholar]
  29. Jackson J. B. 1988; Bacterial photosynthesis. In Bacterial Energy Transduction pp 317–376 Edited by Anthony C. London: Academic Press;
    [Google Scholar]
  30. Jarrett J. T, Amaratunga M, Drennan C. L, Scholten J. D, Sands R. H, Ludwig M. L., Matthews R. G. 1996; Mutations in the B12-binding region of methionine synthase: how the protein controls methylcobalamin reactivity. Biochemistry 35:2464–2475
    [Google Scholar]
  31. Keen N. T, Tamaki S, Kobayashi D., Trollinger D. 1988; Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70:191–197
    [Google Scholar]
  32. Laratta W. P, Choi P. S, Torques I. E., Shapleigh J. P. 2002; Involvement of the PrrB/PrrA two-component system in nitrite respiration in Rhodobacter sphaeroides 2.4.3: evidence of transcriptional regulation. J Bacteriol 184:3521–3529
    [Google Scholar]
  33. Lee J. K., Kaplan S. 1992a; cis -acting regulatory elements involved in oxygen and light control of puc operon transcription in Rhodobacter sphaeroides . J Bacteriol 174:1146–1157
    [Google Scholar]
  34. Lee J. K., Kaplan S. 1992b; Isolation and characterization of trans -acting mutations involved in oxygen regulation of puc operon transcription in Rhodobacter sphaeroides . J Bacteriol 174:1158–1171
    [Google Scholar]
  35. Lenz O, Schwartz E, Dernedde J, Eitinger M., Friedrich B. 1994; The Alcaligenes eutrophus H16 hoxX gene participates in hydrogenase regulation. J Bacteriol 176:4385–4393
    [Google Scholar]
  36. Ludwig M. L., Matthews R. G. 1997; Structure-based perspectives on B12-dependent enzymes. Annu Rev Biochem 66:269–313
    [Google Scholar]
  37. Masuda S., Bauer C. E. 2002; AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides . Cell 110:613–623
    [Google Scholar]
  38. Masuda S, Dong C, Swem D, Setterdahl A. T, Knaff D. B., Bauer C. E. 2002; Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ. Proc Natl Acad Sci U S A 99:7078–7083
    [Google Scholar]
  39. McEwan A. G. 1994; Photosynthetic electron transport and anaerobic metabolism in purple non-sulfur bacteria. Antonie Leeuwenhoek 66:151–164
    [Google Scholar]
  40. Oh J. I., Kaplan S. 2001; Generalized approach to regulation and integration of gene expression. Mol Microbiol 39:1116–1123
    [Google Scholar]
  41. Pemberton J. M., Harding C. M. 1987; Expression of Rhodopseudomonas sphaeroides carotenoid photopigment genes in phylogenetically related non-photosynthetic bacteria. Curr Microbiol 15:67–71
    [Google Scholar]
  42. Pemberton J. M, Horne I. M., McEwan A. G. 1998; Regulation of photosynthetic gene expression in purple bacteria. Microbiology 144:267–278
    [Google Scholar]
  43. Penfold R. J., Pemberton J. M. 1991; A gene from the photosynthetic gene cluster of Rhodobacter sphaeroides induces trans suppression of bacteriochlorophyll and carotenoid levels in R. sphaeroides and R. capsulatus . Curr Microbiol 23:259–263
    [Google Scholar]
  44. Penfold R. J., Pemberton J. M. 1994; Sequencing, chromosomal inactivation and functional expression in Escherichia coli of ppsR , a gene which represses carotenoid and bacteriochlorophyll synthesis in Rhodobacter sphaeroides . J Bacteriol 176:2869–2876
    [Google Scholar]
  45. Pollich M., Klug G. 1995; Identification and sequence analysis of genes involved in late steps in Cbl (vitamin B12) synthesis in Rhodobacter capsulatus . J Bacteriol 177:4481–4487
    [Google Scholar]
  46. Pollich M, Jock S., Klug G. 1993; Identification of a gene required for the oxygen-regulated formation of the photosynthetic apparatus of Rhodobacter capsulatus . Mol Microbiol 10:749–757
    [Google Scholar]
  47. Rödig R, Jock S., Klug G. 1999; Coregulation of the syntheses of bacteriochlorophyll and pigment-binding proteins in Rhodobacter capsulatus . Arch Microbiol 171:198–204
    [Google Scholar]
  48. Roof D. M., Roth J. R. 1992; Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium . J Bacteriol 174:6634–6643
    [Google Scholar]
  49. 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]
  50. Schultz J, Copley R. R, Doerks T, Ponting C. P., Bork P. 2000; smart: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res 28:231–234
    [Google Scholar]
  51. Sheppard D. E., Roth J. R. 1994; A rationale for autoinduction of a transcriptional activator: ethanolamine ammonia-lyase (EutBC) and the operon activator (EutR) compete for adenosyl-cobalamin in Salmonella typhimurium . J Bacteriol 176:1287–1296
    [Google Scholar]
  52. Simon R, Priefer U., Puhler A. 1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/Technology 1:784–791
    [Google Scholar]
  53. Stubbe J. 1994; Binding structure revealed of nature's most beautiful cofactor. Science 266:1663–1664
    [Google Scholar]
  54. Suwanto A., Kaplan S. 1989; Physical and genetic mapping of the Rhodobacter sphaeroides 2.4.1 genome: genome size, fragment identification, and gene localization. J Bacteriol 171:5850–5859
    [Google Scholar]
  55. Thompson J. D, Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
    [Google Scholar]
  56. van Neil C. B. 1944; The culture, general physiology, morphology, and classification of the non-sulfur purple and brown bacteria. Bacteriol Rev 8:1–118
    [Google Scholar]
  57. Yeliseev A. A., Kaplan S. 1995; A sensory transducer homologous to the mammalian peripheral benzodiazepine receptor regulates photosynthetic membrane formation in Rhodobacter sphaeroides 2.4.1. J Biol Chem 270:21167–21175
    [Google Scholar]
  58. Zeilstra-Ryalls J., Kaplan S. 1995; Aerobic and anaerobic regulation in Rhodobacter sphaeroides 2.4.1: the role of the fnrL gene. J Bacteriol 177:6422–6431
    [Google Scholar]
  59. Zeilstra-Ryalls J., Kaplan S. 1998; Role of the fnrL gene in photosystem gene expression and photosynthetic growth of Rhodobacter sphaeroides 2.4.1. J Bacteriol 180:1496–1503
    [Google Scholar]
  60. Zeilstra-Ryalls J, Gomelsky M, Eraso J. M, Yeliseev A, O'Gara J., Kaplan S. 1998; Control of photosystem formation in Rhodobacter sphaeroides . J Bacteriol 180:2801–2809
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.25972-0
Loading
/content/journal/micro/10.1099/mic.0.25972-0
Loading

Data & Media loading...

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