1887

Abstract

Purple phototrophic bacteria have the ability to capture and use sunlight efficiently as an energy source. In these organisms, photosynthesis is carried out under anaerobic conditions. The introduction of oxygen into a culture growing phototrophically results in a rapid decrease in the synthesis of components of the photosynthetic apparatus and a change to an alternative source of energy, usually derived from the degradation of organic compounds under aerobic conditions (chemoheterotrophy). Switching back and forth between anaerobic (photosynthetic) and aerobic growth requires tight regulation of photosynthetic gene expression at the molecular level. Initial experiments by Cohen-Bazire . (1957) showed quite clearly that the regulation of photosynthetic gene expression was in response to two environmental stimuli. The most potent stimulus was oxygen; its presence shut down production of photosynthetic pigments very rapidly. To a lesser extent photosynthetic gene expression responded to light intensity. Low light intensity produced high levels of photosynthetic pigments; high light intensities caused a decrease, but the effect was less dramatic than that observed for oxygen. Since these initial observations were made in some forty years ago, a great deal has been revealed as to the nature of the genes that encode the various components of the photosynthetic apparatus. Recent progress in the understanding of the regulation of expression of these genes in and is the subject of this review.

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1998-02-01
2024-04-25
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References

  1. Armstrong G. A., Alberti M., Leach F., Hearst J. E. 1989; Nucleotide sequence, organization and nature of the protein products of the carotenoid biosynthesis gene cluster of Rhodobacter capsulatus . Mol Gen Genet 216:254–268
    [Google Scholar]
  2. Bauer C. E., Buggy J. J., Yang Z., Marrs B. L. 1991; The superoperonal organization of genes for pigment biosynthesis and reaction center proteins is a conserved feature in Rhodobacter capsulatus: analysis of overlapping bchB and puhA transcripts.. Mol Gen Genet 228:433–444
    [Google Scholar]
  3. Beinert H., Kiley P. J. 1996; Redox control of gene expression involving iron-sulfur proteins. Change of oxidation-state or assembly/disassembly of the Fe-S clusters?. FEBS Lett 382:218–219
    [Google Scholar]
  4. Berks B. C., Ferguson S. J., Moir J. W. B., Richardson D. J. 1995; Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxy- anions.. Biochim Biophys Acta 1232:97–173
    [Google Scholar]
  5. Biel S. W., Wright M. S., Biel A. J. 1988; Cloning of the Rhodobacter capsulatus hemA gene.. J Bacteriol 170:4832–4834
    [Google Scholar]
  6. Bollivar D. W., Suzuki J. Y., Beatty J. T., Dobrowski J., Bauer C. E. 1994; Directed mutagenesis of bacteriochlorophyll a biosynthesis in Rhodobacter capsulatus . J Mol Biol 237:622–640
    [Google Scholar]
  7. Buggy J., Bauer C. E. 1995; Cloning and characterization of senC, a gene involved in both aerobic respiration and photosynthesis gene expression in Rhodobacter capsulatus . J Bacteriol 177:6958–6965
    [Google Scholar]
  8. Buggy J., Sganga M. W., Bauer C. E. 1994a; Nucleotide sequence and characterization of the Rhodobacter capsulatus hvrB gene: HvrB is an activator of S-adenosyl-L-homocysteine hydrolase expression and is a member of the LysR family.. J Bacteriol 176:61–69
    [Google Scholar]
  9. Buggy J., Sganga M. W., Bauer C. E. 1994b; Characterization of a light-responding trans-activtator responsible for differentially controlling reaction center and light-harvesting I gene expression in Rhodobacter capsulatus . J Bacteriol 176:6936–6943
    [Google Scholar]
  10. 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]
  11. Coomber S. A., Hunter C. N. 1989; Construction of a physical map of the 45 kb photosynthetic gene cluster of Rhodobacter sphaeroides . Arch Microbiol 151:454–458
    [Google Scholar]
  12. Coomber S. A., Chaudhri M., Connor A., Britton G., Hunter C. N. 1990; Localized transposon Tn5 mutagenesis of the photosynthetic gene cluster of Rhodobacter sphaeroides . Mol Microbiol 4:977–989
    [Google Scholar]
  13. Coomber S. A., Jones R. M., Jordan P. M., Hunter C. N. 1992; A putative anaerobic coproporphyrinogen lll oxidase in Rhodobacter sphaeroides. I. Molecular cloning, transposon mutagenesis and sequence analysis of the gene.. Mol Microbiol 6:3159–3169
    [Google Scholar]
  14. Dispensa M., Thomas C., Kim M.-K., Perrotta J. A., Gibson J. B., Harwood C. S. 1992; Anaerobic growth of Rhodopseudomonas palustris on 4-hydroxybenzoate is dependent of AadR, a member of the cyclic AMP receptor class of transcriptional regulators.. J Bacteriol 174:5803–5813
    [Google Scholar]
  15. Dobbin P. S., Warren L. H., Cook N. J., McEwan A. G., Powell A. K., Richardson D. J. 1996; Dissimilatory iron(III) reduction by Rhodobacter capsulatus . Microbiology 142:765–774
    [Google Scholar]
  16. Elsen S., Richaud P., Colbeau A., Vignais P. M. 1993; Sequence analysis and interposon mutagenesis of the hupT gene, which encodes a sensor protein involved in repression of hydrogenase synthesis in Rhodobacter capsulatus . J Bacteriol 175:7404–7412
    [Google Scholar]
  17. 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]
  18. Eraso J. M., Kaplan S. 1995; Oxygen-insensitive synthesis of photosynthetic membranes of Rhodobacter sphaeroides: a mutant histidine kinase.. J Bacteriol 177:2695–2706
    [Google Scholar]
  19. Fuerst J. A., Hawkins J. A., Holmes A., Sly L. I., Moore C. J., Stackebrandt E. 1993; Porphyrobacter neustonensis gen. nov., sp. nov., an aerobic bacteriochlorophyll-synthesizing budding bacterium from fresh water.. Int J Syst Bacteriol 43:125–134
    [Google Scholar]
  20. Garcia-Horsman J. A., Barquera B., Rumbley J., Ma J., Gennis R. B. 1994; The superfamily of heme-copper respiratory oxidases.. J Bacteriol 176:5587–5600
    [Google Scholar]
  21. Gicquel-Sanzey B., Cossart P. 1982; Homologies between different procaryotic DNA-binding regulatory proteins and between their sites of action.. EMBO J 1:591–595
    [Google Scholar]
  22. Glerum D. M., Shtank A., Tzagoloff A. 1996; SCO1 and SC02 act as high copy number suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae . J Biol Chem 271:20531–20535
    [Google Scholar]
  23. 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]
  24. 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]
  25. Gomelsky M., Kaplan S. 1997; Molecular genetic analysis suggesting interactions between AppA and PpsR in regulation of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1.. J Bacteriol 179:128–134
    [Google Scholar]
  26. Griffiths M., Stanier R. Y. 1956; Some mutational changes in the photosynthetic pigment systems of Rhodopseudomonas spheroides . J Gen Microbiol 14:698–715
    [Google Scholar]
  27. Gussin G. N., Ronson C. W., Ausubel F. M. 1986; Regulation of nitrogen fixation genes.. Annu Rev Genet 20:567–591
    [Google Scholar]
  28. Hobbs M., Collie E. S. R., Free P. D., Livingston S. P., Mattick J. P. 1993; PilS and PilR, a two-component transcriptional regulatory system controlling expression of type-1 fimbriae in Pseudomonas aeruginosa . Mol Microbiol 7:669–682
    [Google Scholar]
  29. Hornberger U., Liebetanz R., Tichy H. V., Drews G. 1990; Cloning and sequencing of the hemA gene of Rhodobacter capsulatus and isolation of a delta-aminolevulinic acid-dependent mutant strain.. Mol Gen Genet 221:371–378
    [Google Scholar]
  30. 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]
  31. Hunter C. N., McGlynn P., Ashby M. K., Burgess J. G., Olsen J. D. 1991; DNA sequencing and complementation/deletion analysis of the bchA-puf operon region of Rhodobacter sphaeroides : in vivo mapping of the oxygen-regulated puf promoter.. Mol Microbiol 5:2649–2661
    [Google Scholar]
  32. Inoue K., Kouadio J. L., Mosley C. S., Bauer C. E. 1995; Isolation and in vitro phosphorylation of sensory transduction components controlling anaerobic induction of light harvesting and reaction center gene expression in Rhodobacter capsulatus . Biochemistry 34:391–396
    [Google Scholar]
  33. Iuchi S., Linn E. C. C. 1995 Signal transductions in the Arc system for control of operons encoding aerobic respiratory enzymes.. In Two-component Signal Transduction pp 223–231 Edited by Hoch J. H., Silhavy T. J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  34. Jackson J. B. 1988 Bacterial photosynthesis.. In Bacterial Energy Transduction pp 317–376 Edited by Anthony C. London: Academic Press;
    [Google Scholar]
  35. Joshi H. M., Tabita F. R. 1996; A global, two component signal transduction system that integrates the control of photosynthesis, carbon dioxide fixation and nitrogen fixation.. Proc Natl Acad Sci USA 93:14515–14520
    [Google Scholar]
  36. Khoroshilova N., Popescu C., Munck E., Beinert H., Kiley P. J. 1997; Iron-sulfur cluster dissassembly in the Fnr protein of Escherichia coli by O2: [4Fe−4S] to [2Fe−2S] conversion with loss of biological acitivity.. Proc Nat Acad Sci USA 94:6087–6092
    [Google Scholar]
  37. Kiley P. J., Kaplan S. 1988; Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter spbaeroides . Microbiol Rev 52:50–69
    [Google Scholar]
  38. Kiley P. J., Reznikoff W. S. 1991; Fnr mutants that activate gene expression in the presence of oxygen.. J Bacteriol 173:16–22
    [Google Scholar]
  39. Kirndorfer M., Hebermehl M., Hemschemeier K., Jager A., Ebel U., Klug G. 1997; Transcriptional regulation of puf and puc operon expression in Rhodobacter capsulatus by the DNA binding proteins RegA and IHF.. Abstracts of the 9th International Symposium on Phototrophic Prokaryotes, Vienna p. 69
    [Google Scholar]
  40. Lang H. P., Cogdell R. J., Takaichi S., Hunter C. N. 1995; Complete DNA sequence, specific Tn5 insertion map, and gene assignment of the carotenoid biosynthesis pathway of Rhodobacter spbaeroides . J Bacteriol 177:2064–2073
    [Google Scholar]
  41. Lascelles J., Wertlieb D. 1971; Mutant strains of Rhodo-pseudomonas spbaeroides which form photosynthetic pigments aerobically in the dark; growth characteristics and enzymic activities.. Biochim Biophys Acta 226:328–340
    [Google Scholar]
  42. Lazazzera B. A., Beinert H., Khoroshilova N., Kennedy M. C., Kiley P. J. 1996; DNA binding and dimerization of the Fe–S containing FNR protein from Escherichia coli are regulated by oxygen.. J Biol Chem 271:2762–2768
    [Google Scholar]
  43. Lee J. K., Kaplan S. 1992; Isolation and characterisation of trans-acting mutations involved in oxygen regulation of puc operon transcription in Rhodobacter spbaeroides . J Bacteriol 174:1158–1171
    [Google Scholar]
  44. Masepohl B., Klipp W. 1996; Organization and regulation of genes encoding the molybdenum nitrogenase and the alternative nitrogenase in Rhodobacter capsulatus . Arch Microbiol 165:80–90
    [Google Scholar]
  45. Monson E. K., Weinstein M., Ditta G. S., Helinski D. R. 1992; The FixL protein of Rhizobium meliloti can be separated into a heme-binding oxygen sensing domain and a functional C-terminal kinase domain.. Proc Natl Acad Sci USA 89:4280–4284
    [Google Scholar]
  46. Mosley C. S., Suzuki J. Y., Bauer C. E. 1994; Identification and molecular characterisation of a sensor histidine kinase responsible for coordinately regulating light harvesting and reaction center gene expression in response to anaerobiosis.. J Bacteriol 176:7566–7573
    [Google Scholar]
  47. Neidle E. L., Kaplan S. 1993; Expression of the Rhodobacter spbaeroides hemA and hemT genes, encoding two 5-amino- levulinic acid synthase enzymes.. J Bacteriol 175:2292–2303
    [Google Scholar]
  48. OʹGara J. P., Kaplan S. 1997; Evidence for the role of redox carriers in photosynthesis gene expression and carotenoid biosynthesis in Rhodobacter spbaeroides 2.4.1.. J Bacteriol 179:1951–1961
    [Google Scholar]
  49. Parkinson J. S. 1993; Signal transduction schemes of bacteria.. Cell 73:857–871
    [Google Scholar]
  50. Pasloske B. L., Drummond D. S., Frost L. S., Paranchych W. 1989; The activity of the Pseudomonas aeruginosa pilin promoter is enhanced by an upstream regulatory site.. Gene 81:25–34
    [Google Scholar]
  51. Pemberton J. M., Bowen A. R., St G. 1981; High frequency chromosome transfer in Rhodopseudomonas spbaeroides promoted by the broad host range plasmid RPl carrying the mercury transposon Tn501.. J Bacteriol 147:110–117
    [Google Scholar]
  52. Penfold R. J., Pemberton J. M. 1991; A gene from the photosynthetic cluster of Rhodobacter spbaeroides induces trans suppression of bacteriochlorophyll and carotenoid levels in R. spbaeroides and R. capsulatus . Curr Microbiol 23:259–263
    [Google Scholar]
  53. 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 spbaeroides . J Bacteriol 176:2869–2876
    [Google Scholar]
  54. Phillips-Jones M. K., Hunter C. N. 1994; Cloning and nucleotide sequence of regA, a putative response regulator gene of Rhodobacter spbaeroides . FEMS Microbiol Lett 116:269–276
    [Google Scholar]
  55. Ponnampalam S. N., Buggy J. J., Bauer C. E. 1995; Characterization of an aerobic repressor that coordinately regulates bacteriochlorophyll, carotenoid, and light harvesting-II expression in Rhodobacter capsulatus . J Bacteriol 177:2990–2997
    [Google Scholar]
  56. Poole R. K. 1994; Oxygen reactions with bacterial oxidases and globins: binding, reduction and regulation.. Antonie van Leeuwenhoek 65:289–310
    [Google Scholar]
  57. Pratt L. A., Silhavy T. J. 1995 Porin regulon of Eshcerichia coli . In Two-component Signal Transduction pp 105–127 Edited by Hoch J. H., Silhavy T. J. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  58. Preisig O., Zufferey R., Hennecke H. 1996; The Brady-rhizobium japonicum fixGHIS genes are required for the formation of the high-affinity cbb3-type cytochrome oxidase.. Arch Microbiol 165:297–305
    [Google Scholar]
  59. Qian Y., Tabita F. R. 1996; A global signal transduction system regulates aerobic and anaerobic CO2 fixation in Rhodobacter spbaeroides . J Bacteriol 178:12–18
    [Google Scholar]
  60. Ramakrishnan G., Newton A. 1990; FlbD of Caulobacter crescentus is a homologue of the NtrC (NRI) protein and activates σ54-dependent flagellar gene promoters.. Proc Natl Acad Sci USA 87:2369–2373
    [Google Scholar]
  61. Richardson D. J., McEwan A. G., Jackson J. B., Ferguson S. J. 1989; Electron transport pathways to nitrous oxide in Rhodobacter species.. Eur J Biochem 185:659–669
    [Google Scholar]
  62. Richardson D. J., Bell L., G, McEwan A. G., Jackson J. B., Ferguson S. J. 1991; Cytochrome c 2 is essential for electron transfer to nitrous oxide reductase from physiological substrates in Rhodobacter capsulatus and can act as an electron donor in vitro . Eur J Biochem 199:677–683
    [Google Scholar]
  63. Schulze M., Rodel G. 1989; Accumulation of the cytochrome c oxidase subunits I and ll in yeast requires a mitochondrial membrane-associated protein, encoded by the nuclear scol gene.. Mol Gen Genet 68:945–954
    [Google Scholar]
  64. Sganga M. W., Bauer C. E. 1992; Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus . Cell 68:945–954
    [Google Scholar]
  65. Sganga M. W., Aksamit R. R., Cantoni G. L., Bauer G E. 1992; Mutational and nucleotide sequence analysis of S-adenosyl-L-homocysteine hydrolase from Rhodobacter capsulatus . Proc Natl Acad Sci USA 89:6328–6332
    [Google Scholar]
  66. Shimada H., Iba K., Takimiya K. 1992; Blue light irradiation reduces the expression of puf and puc operons of Rhodobacter sphaeroides under semi-aerobic conditions.. Plant Cell Physiol 33:471–475
    [Google Scholar]
  67. Shimada H., Ohta H., Masuda T., Shioi Y., Takimiya K. 1993; A putative transcription factor binding to the upstream region of the puf operon in Rhodobacter sphaeroides . FEBS Lett 328:41–44
    [Google Scholar]
  68. Shimada H., Wada T., Handa H., Ohta H., Mizoguchi H., Nishimura K., Masuda T., Shioi Y., Takimiya K. 1996; A transcription factor with a leucine-zipper motif involved in light-dependent inhibition of expression of the puf operon in the photosynthetic bacterium Rhodobacter sphaeroides . J Bacteriol 37:512–522
    [Google Scholar]
  69. Spiro S. 1994; The Fnr family of transcriptional regulators.. Antonie van Leeuwenhoek 66:23–36
    [Google Scholar]
  70. Suwanto A., Kaplan S. 1989; Physical and genetic mapping of the Rhodobacterer sphaeroiides 2.4.1 genome: genome size, fragment identification and gene localization.. J Bacteriol 171:5840–5849
    [Google Scholar]
  71. Taylor D. P., Cohen S. N., Clark W. G., Marrs B. L. 1983; Alignment of genetic and restriction maps of the photosynthesis region of the Rhodopseudomonas capsulata chromosome by a conjugation-mediated marker rescue technique.. J Bacteriol 154:580–590
    [Google Scholar]
  72. Tokito M. K., Daldal F. 1992; petR, located upstream of the fbdFBC operon encoding the cytochrome bcl complex, is homologous to bacterial response regulators and necessary for photosynthetic and respiratory growth of Rhodobacter capsulatus . Mol Microbiol 6:1645–1654
    [Google Scholar]
  73. Unden G., Trageser M., Duchene A. 1990; Effect of positive redox potentials ( + 400mV) on the expression of anaerobic respiratory enzymes in Escherichia coli . Mol Microbiol 4:315–319
    [Google Scholar]
  74. van Waasbergen L. G., Hildebrand M., Tebo B. M. 1996; Identification and characterisation of a gene cluster involved in manganese oxidation by spores of the marine Bacillus sp. strain SG-1.. J Bacteriol 178:3517–3530
    [Google Scholar]
  75. Wellington C. L., Bauer C. E., Beatty J. T. 1992; Photosynthesis gene superoperons in purple nonsulfur bacteria: the tip of the iceberg?. Can J Microbiol 38:20–27
    [Google Scholar]
  76. Willison J. C., Ahombo G., Chabert J., Magnin J. P., Vignais P. M. 1985; Genetic mapping of the Rhodopseudomonas capsulata chromosome shows non-clustering of genes involved in nitrogen fixation.. J Gen Microbiol 131:3001–3015
    [Google Scholar]
  77. Yeliseev A. A., Kaplan S. 1995; A sensory transducer homologous to the mammalian peripheral-type benzodiazepine receptor regulates photosynthetic membrane complex formation in Rhodobacter sphaeroides 2.4.1.. J Biol Chem 270:21167–21175
    [Google Scholar]
  78. Yen H. C., Marrs B. L. 1976; Map of genes for carotenoid and bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata . J Bacteriol 126:619–629
    [Google Scholar]
  79. Yildiz F. H., Gest H., Bauer C. E. 1991; Genetic analysis of photosynthesis in Rhodospirillum centenum . J Bacteriol 173:4163–4170
    [Google Scholar]
  80. Yildiz F. H., Gest H., Bauer C. E. 1992; Conservation of the photosynthesis gene cluster in Rhodospirillum centenum . Mol Microbiol 6:2683–2691
    [Google Scholar]
  81. 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]
  82. Zeilstra-Ryalls J., Kaplan S. 1996; Control of hemA expression in Rhodobacter sphaeroides 2.4.1: regulation through alterations in the cellular redox state.. J Bacteriol 178:985–993
    [Google Scholar]
  83. Ziegelhoffer E. C., Kiley P. J. 1995; In vitro analysis of a constitutively active mutant form of the Escherichia coli global transcription factor FNR.. J Mol Biol 245:351–361
    [Google Scholar]
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