1887

Abstract

The temporal expression of ten clustered genes required for carotenoid () and bacteriochlorophyll () biosynthesis was examined during the transition from aerobic respiration to anaerobiosis requisite for the development of the photosynthetic membrane in the bacterium . Accumulation of and mRNAs increased transiently and coordinately, up to 12-fold following removal of oxygen from the growth medium, paralleling increases in mRNAs encoding pigment-binding polypeptides of the photosynthetic apparatus. The and genes, in contrast, were expressed similarly in the presence or absence of oxygen. The regulation patterns of promoters for the and genes and the operon were characterized using transcriptional fusion and qualitatively reflected the corresponding mRNA accumulation patterns. We also report that the gene product, encoded by a DNA sequence previously considered to be a portion of , shares 49% sequence identity with the nuclear-encoded Cs chloroplast protein required for normal pigmentation in plants.

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1993-05-01
2024-04-18
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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. Molecular and General Genetics 216:254–268
    [Google Scholar]
  2. Armstrong G. A., Alberti M., Hearst J. E. 1990a; Conserved enzymes mediate the early reactions of carotenoid biosynthesis in nonphotosynthetic and photosynthetic prokaryotes. Proceedings of the National Academy of Sciences of the United States of America 87:9975–9979
    [Google Scholar]
  3. Armstrong G. A., Alberti M., Leach F., Hearst J. E. 1990b; Organization of the Rhodobacter capsulatus carotenoid biosynthesis gene cluster. In Molecular Biology of Membrane-Bound Complexes in Phototrophic Bacteria pp. 39–46 Drews G., Dawes E. Edited by New York: Plenum Press;
    [Google Scholar]
  4. Armstrong G. A., Schmidt A., Sandmann G., Hearst J. E. 1990c; Genetic and biochemical characterization of carotenoid biosynthesis mutants of Rhodobacter capsulatus. Journal of Biological Chemistry 265:8329–8338
    [Google Scholar]
  5. Baker M. E., Fanestil D. D. 1991; Mammalian peripheral-type benzodiazepine receptor is homologous to CrtK protein of Rhodobacter capsulatus, a photosynthetic bacterium. Cell 65:721–722
    [Google Scholar]
  6. Bartley G. E., Scolnik P. A. 1989; Carotenoid biosynthesis in photosynthetic bacteria. Journal of Biological Chemistry 264:13109–13113
    [Google Scholar]
  7. Bartley G. E., Schmidhauser T. J., Yanofsky C., Scolnik P. A. 1990; Carotenoid desaturases from Rhodobacter capsulatus and Neurospora crassa are structurally and functionally conserved and contain domains homologous to flavoprotein disulfide oxidoreductases. Journal of Biological Chemistry 265:16020–16024
    [Google Scholar]
  8. Belasco J. G., Beatty J. T., Adams C. W., von Gabain A., Cohen S. N. 1985; Differential expression of photosynthesis genes in R. capsulata results from segmental differences in stability within the polycistronic rxcA transcript. Cell 40:171–181
    [Google Scholar]
  9. Biel A. J., Marrs B. L. 1983; Transcriptional regulation of several genes for bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata in response to oxygen. Journal of Bacteriology 156:686–694
    [Google Scholar]
  10. Biel A. J., Marrs B. L. 1985; Oxygen does not directly regulate carotenoid biosynthesis in Rhodopseudomonas capsulata. Journal of Bacteriology 162:1320–1321
    [Google Scholar]
  11. Bramley P. M., Mackenzie A. 1988; The regulation of carotenoid biosynthesis. In Current Topics in Cellular Regulation 29 pp. 291–343 Horecker B. L., Stadtman E. R. Edited by London: Academic Press;
    [Google Scholar]
  12. Burke D. H., Alberti M., Armstrong G. A., Hearst J. E. 1991a; The complete nucleotide sequence of the 46 kb photosynthesis gene cluster of Rhodobacter capsulatus. EMBL Data Library, accession number Z11165
    [Google Scholar]
  13. Burke D., Alberti M., Stein D., Hearst J. E. 1991b; Chlorophyll Fe proteins and other chlorophyll biosynthesis genes from Rhodobacter capsulatus to higher plants, abstract T/pm-B5. Abstract from the 19th Annual Meeting of the American Society for Photobiology. Photochemistry and Photobiology 53:85S
    [Google Scholar]
  14. Castelfranco P. A., Beale S. I. 1983; Chlorophyll biosynthesis: recent advances and areas of current interest. Annual Review of Plant Physiology 34:241–278
    [Google Scholar]
  15. Chamovitz D., Misawa N., Sandmann G., Hirschberg J. 1992; Molecular cloning and expression in Escherichia coli of a cyanobacterial gene coding for phytoene synthase, a carotenoid biosynthesis enzyme. FEBS Letters 296:305–310
    [Google Scholar]
  16. Chen C. -Y. A., Beatty J. T., Cohen S. N., Belasco J. G. 1988; An intercistronic stem-loop structure functions as an mRNA decay terminator necessary but insufficient for puf mRNA stability. Cell 52:609–619
    [Google Scholar]
  17. Clark W. G, Davidson E., Marrs B. L. 1984; Variations of mRNA levels coding for antenna and reaction center polypeptides in Rhodopseudomonas capsulata in response to changes in oxygen concentration. Journal of Bacteriology 157:945–948
    [Google Scholar]
  18. Cogdell R. J., Frank H. A. 1987; How carotenoids function in photosynthetic bacteria. Biochimica et Biophysica Acta 895:63–79
    [Google Scholar]
  19. Cohen-Bazire G., Sistrom W. R., Stanier R. Y. 1957; Kinetic studies of pigment synthesis by non-sulfur purple bacteria. Journal of Cellular and Comparative Physiology 49:25–68
    [Google Scholar]
  20. Cook D. N., Armstrong G. A., Hearst J. E. 1989; Induction of anaerobic gene expression in Rhodobacter capsulatus is not accompanied by a local change in chromosomal supercoiling as measured by a novel assay. Journal of Bacteriology 171:4836–4843
    [Google Scholar]
  21. Coomber S. A., Chaudri M., Connor A., Britton G., Hunter C. N. 1990; Localized transposon Tn5 mutagenesis of the photosynthetic gene cluster of Rhodobacter sphaeroides. Molecular Micro-biology 4:977–989
    [Google Scholar]
  22. Demmig-Adams B. 1990; Carotenoids and photoprotection in plants: a role for the xanthophyll zeaxanthin. Biochimica et Biophysica Acta 1020:1–24
    [Google Scholar]
  23. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Research 12:387–395
    [Google Scholar]
  24. Ditta G., Stanfield S., Corbin D., Helinski D. R. 1980; Broad host range DNA cloning system for Gram-negative bacteria: construction of a gene bank of Rhizobium meliloti. Proceedings of the National Academy of Sciences of the United States of America 77:7347–7351
    [Google Scholar]
  25. Giuliano G., Pollock D., Stapp H., Scolnik P. A. 1988; A genetic-physical map of the Rhodobacter capsulatus carotenoid biosynthesis gene cluster. Molecular and General Genetics 213:78–83
    [Google Scholar]
  26. Golecki J. R., Schumacher A., Dnrws G. 1980; The differentiation of the photosynthetic apparatus and the intracytoplasmic membrane in cells of Rhodopseudomonas capsulata upon variation of light intensity. European Journal of Cell Biology 23:1–5
    [Google Scholar]
  27. Goodwm T. W. 1980 The Biochemistry of the Carotenoids l Plants p. 63 New York: Chapman & Hall;
    [Google Scholar]
  28. Gorchein A. 1973; Control of magnesium protoporphyrin chelatase activity in Rhodospseudomonas spheroides. Biochemical Journal 134:833–845
    [Google Scholar]
  29. Hunter C. N., Coomber S. A. 1988; Cloning and oxygen-regulated expression of the bacteriochlorophyll biosynthesis genes bch E, B, A and C of Rhodobacter sphaeroides. Journal of General Microbiology 134:1491–1497
    [Google Scholar]
  30. Husain I., Van Houten B., Thomas D. C., Sancar A. 1986; Sequences of Escherichia coli uvrA gene and protein reveal two potential ATP binding sites. Journal of Biological Chemistry 261:4895–4901
    [Google Scholar]
  31. Kaufmann N., Reidl H. H., Golecki J. R., Garcia A. F., Drews G. 1982; Differentiation of the membrane system in cells of Rhodopseudomonas capsulata after transition from chemotrophic to phototrophic growth conditions. Archives of Microbiology 131:313–322
    [Google Scholar]
  32. Keister D. L. 1978; Respiration versus photosynthesis. In The Photosynthetic Bacteria pp. 849–856 Clayton R. K., Sistrom W. R. Edited by New York: Plenum Press;
    [Google Scholar]
  33. Kiley P. J., Kaplan S. 1988; Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. Microbiological Reviews 52:56–69
    [Google Scholar]
  34. Klug G., Kaufmann N., Drews G. 1985; Gene expression of pigment-binding proteins of the bacterial photosynthetic apparatus: transcription and assembly in the membrane of Rhodopseudomonas capsulata. Proceedings of the National Academy of Sciences of the United States of America 82:6485–6489
    [Google Scholar]
  35. Koncz C., Mayerhofer R., Koncz-Kalman Z., Nawrath C., Reiss B., Redei G. P., Schell J. 1990; Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana. EMBO Journal 9:1337–1346
    [Google Scholar]
  36. Krinsky N. I. 197l; Function. In Carotenoids pp. 669–716 Isler O., Gutmann H., Solms U. Edited by Basel, Switzerland: Birkhäuser Verlag;
    [Google Scholar]
  37. Leach F., Armstrong G. A., Hearst J. E. 1991; Photosynthesis genes in Rhodobacter capsulatus can be regulated by oxygen during dark respiratory growth with DMSO. Journal of General Microbiology 137:1551–1556
    [Google Scholar]
  38. Ma D., Cook D. N., O’Brien D. A., Hewst J. E. 1993; Analysis of the promoter and regulatory sequences of an oxygen-regulated bch gene in Rhodobacter capsulatus by site-directed mutagenesis. Journal of Bacteriology in the press
    [Google Scholar]
  39. Marrs B. 1981; Mobilization of the genes for photosynthesis from Rhodopseudomonas capsulata by a promiscuous plasmid. Journal of Bacteriology 146:1003–1012
    [Google Scholar]
  40. Math S. K., Hearst J. E., Poulter C. D. 1992; The crtE gene in Erwinia herbicola encodes geranylgeranyl diphosphate synthase. Proceedings of the National Academy of Sciences of the United States of America 89:6761–6764
    [Google Scholar]
  41. Miller J. H. 1972 Experiments in Molecular Genetics pp. 352–355 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  42. van Niel C. B. 1944; The culture, general physiology, morphology and classification of the nonsulfur purple and brown bacteria. Bacteriological Reviews 8:1–118
    [Google Scholar]
  43. Oka A., Sugisaki H., M. Takanami M. 1981; Nucleotide sequence of the kanamycin resistance transposon Tn 903. Journal of Molecular biology 147:217–226
    [Google Scholar]
  44. Orsat B., Monfort A., Chatellard P., Stutz E. 1992; Mapping and sequencing of an actively transcribed Euglena gracilis chloroplast gene (ccs A) homologous to the Arabidopsis thaliana nuclear gene cs (ch-42). FEBS Letters 303:181–184
    [Google Scholar]
  45. Sandmann G., Misawa N. 1992; New functional assignment of the carotenogenic genes crtB and crtE with constructs of these genes from Erwinia species. FEMS Microbiology Letters 90:253–258
    [Google Scholar]
  46. Schumacher A., Drews G. 1978; The formation of bacteriochlorophyll-protein complexes of the photosynthetic apparatus of Rhodopseudomonas capsulata during the early stages of development. Biochimica et Biophysica Acta 501:183–194
    [Google Scholar]
  47. Scolnik P. A., Marrs B. L. 1987; Genetic research with photosynthetic bacteria. Annual Reuiew of Microbiology 41:703–726
    [Google Scholar]
  48. Straub O. 1987 Key to Carotenoids pp. 1–296 Pfander H. Edited by Basel, Switzerland: Birkhäuser Verlag;
    [Google Scholar]
  49. Taylor D. P., Cohen S. N., Clark W. G., Marrs B. L. 1983; Alignment of the genetic and restriction maps of the photosynthesis region of the Rhodopseudomonas capsulata chromosome by a conjugation-mediated marker rescue technique. Journal of Bacteriology 154:580–590
    [Google Scholar]
  50. Vieira J., Messing J. 1982; The pUC plasmids, an M13mp7 derived system for insertion mutagenesis and sequencing with universal primers. Gene 19:259–268
    [Google Scholar]
  51. Walker J., Weinstein J. 1991; In vitro assay of the chlorophyll biosynthetic enzyme Mg-chelatase: Resolution of the activity into soluble and membrane-bound fractions. Proceedings of the National Academy of Sciences of the United States of America 88:5789–5793
    [Google Scholar]
  52. Walker J. E., Saraste M., Runswick M. J., Gra N. J. 1982; Distantly related sequences in the α- and β-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO Journal 8:945–951
    [Google Scholar]
  53. Wellington C. L., Beatty J. T. 1989; Promoter mapping and nucleotide sequence of the bchC bacteriochlorophyll biosynthesis gene from Rhodobacter capsulatus. Gene 83:251–261
    [Google Scholar]
  54. Wellington C. L., Beatty J. T. 1991; Overlapping mRNA transcripts of photosynthesis gene operons in Rhodobacter capsulatus. Journal of Bacteriology 173:1432–1443
    [Google Scholar]
  55. Yang Z., Bauer C. E. 1990; Rhodobacter capsulatus genes involved in early steps of the bacteriochlorophyll biosynthetic pathway. Journal of Bacteriology 172:5001–5010
    [Google Scholar]
  56. Yen H. C., Marrs B. 1976; Map of genes for carotenoid and bacteriochlorophyll biosynthesis in Rhodopseudomonas capsulata. Journal of Bacteriology 126:619–629
    [Google Scholar]
  57. Young D. A., Bauer C. E., Williams J. C., Marrs B. L. 1989; Genetic evidence for superoperonal organization of genes for photosynthetic pigments and pigment-binding proteins in Rhodobacter capsulatus. Molecular and General Genetics 218:1–12
    [Google Scholar]
  58. Yu P. L., Hohn B., Falk H., Drews G. 1982; Molecular cloning of the ribosomal RNA genes of the photosynthetic bacterium Rhodopseudomonas capsulata. Molecular and General Genetics 188:392–398
    [Google Scholar]
  59. Zhu Y. S., Hearst J. E. 1986; Regulation of the expression of the genes for light-harvesting antenna proteins LH-I and LH-II ; reaction center polypeptides RC-L, RC-M, and RC-H; and enzymes of bacteriochlorophyll and carotenoid biosynthesis in Rhodobacter capsulatus by light and oxygen. Proceedings of the National Academy of Sciences of the United States of America 83:7613–7617
    [Google Scholar]
  60. Zhu Y. S., Kaplan S. 1985; Effects of light, oxygen, and substrates on steady-state levels of mRNA coding for ribu1ose-1,5-bisphosphate carboxylase and light-harvesting and reaction center polypeptides in Rhodopseudomonas sphaeroides. Journal of Bacteriology 162:925–932
    [Google Scholar]
  61. Zsebo K. M. 1984 Genetic-physical mapping ofa photosynthetic gene cluster in Rhodopseudomonas capsulata PhD thesis University of California, Berkeley USA:
    [Google Scholar]
  62. Zsebo K. M., Hearst J. E. 1984; Genetic-physical mapping of a photosynthetic gene cluster from R capsulata. Cell 37:937–947
    [Google Scholar]
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