Structure of the puf operon of the obligately aerobic, bacteriochlorophyll a-containing bacterium Roseobacter denitrificans OCh114 and its expression in a Rhodobacter capsulatus puf puc deletion mutant

Journal of Bacteriology

Volumn 179, Issue 17, 1997, Pages 5247-5258

  Kortlüke, Christiane ^a   Breese, Klaus ^a   Gad'on, Nasser ^a   Labahn, Andreas ^a   Drews, Gerhart ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; GENE EXPRESSION; GENE STRUCTURE; NONHUMAN; OPERON; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; RHODOBACTER CAPSULATUS;

BACTERIA (MICROORGANISMS); CHLOROFLEXUS AURANTIACUS; ERYTHROBACTER; ESCHERICHIA COLI; PHOTOBACTERIA; PROTEOBACTERIA; RHODOBACTER CAPSULATUS; RHODOBACTER DENITRIFICANS; RHODOPSEUDOMONAS; ROSEOBACTER DENITRIFICANS; RUBRIVIVAX GELATINOSUS;

EID: 0346414462     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.17.5247-5258.1997     Document Type: Article

References (70)

1. Barz, W. P., F. Francia, G. Venturoli, B. A. Melandri, A. Vermeglio, and D. Oesterhelt. 1995. Role of PufX protein in photosynthetic growth of Rb. sphaeroides. I. Biochemistry 34:15235-15247.
2. Barz, W. P., A. Vermeglio, F. Francia, G. Venturoli, B. A. Melandri, and D. Oesterhelt. 1995. Role of PufX protein in photosynthetic growth of Rb. sphaeroides. II. Biochemistry 34:15248-15258.
3. Bauer, C. E. 1995. Regulation of photosynthesis gene expression, p. 1221-1234. In R. E. Blankenship, M. T. Madigan, and C. E. Bauer (ed.), Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
4. Bauer, C. E., and B. L. Marrs. 1988. Rhodobacter capsulatus puf operon encodes a regulatory protein (PufQ) for bacteriochlorophyll biosynthesis. Proc. Natl. Acad. Sci. USA 85:7074-7078.
5. Bauer, C. E., D. A. Young, and B. L. Marrs. 1988. Analysis of the Rhodobacter capsulatus puf operon. J. Biol. Chem. 263:4820-4827.
6. Blake, M. S., K. H. Johnston, G. J. Russell-Jones, and E. C. Gotschlich. 1984. A rapid, sensitive method for detection of alkaline phosphatase-conjugated anti-antibody on western blots. Anal. Biochem. 136:175-179.
7. Bullock, W. O., J. M. Fernandez, and J. M. Short. 1987 XL1-Blue, a high efficiency plasmid transforming recA Escherichia coli strain with beta-galactosidase selection. BioTechniques 5:376-379.
8. Debus, R. J., G. Feher, and M. Y. Okamura. 1985. LM complex of reaction centers from Rhodopseudomonas sphaeroides R 26: characterization and reconstitution with the H subunit. Biochemistry 24:2488-2500.
9. Dracheva, S., J. C. Williams, G. van Driesche, J. J. van Beeumen, and R. E. Blankenship. 1991. The primary structure of cytochrome c554 from the green photosynthetic bacterium Chloroflexus aurantiacus. Biochemistry 30: 11451-11458.
10. Drews, G. 1983. Mikrobiologisches Praktikum, 4th ed., p. 62. Springer Verlag, Berlin, Germany.
11. Drews, G. 1996. Formation of the light-harvesting complex I (B870) of anoxygenic phototrophic purple bacteria. Arch. Microbiol. 166:151-159.
12. Drews, G., and J. R. Golecki. 1995. Structure, molecular organization and biosynthesis of membranes of purple bacteria, p. 231-257. In R. E. Blankenship, M. T. Madigan, and C. E. Bauer (ed.), Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
13. Erasco, J. M., and S. Kaplan. 1996. Complex regulatory activities associated with the histidine kinase PrrB in expression of photosynthesis genes in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 178:7037-7046.
14. Farchaus, J. W., W. P. Barz, H. Grünberg, and D. Oesterhelt. 1992. Studies on the expression of the pufX polypeptide and the requirement for photoheterotrophic growth in Rhodobacter sphaeroides. EMBO J. 11:2779-2788.
15. Feher, G., J. P. Allen, M. Y. Okamura, and D. C. Rees. 1989. Structure and function of bacterial photosynthetic reaction centers. Nature 339:111-116.
16. Ferguson, S. J., J. B. Jackson, and A. G. McEvan. 1987. Anaerobic respiration in the Rhodospirillaceae: characterization of pathways and evaluation of roles in redox balancing during photosynthesis. FEMS Microbiol. Rev. 46: 117-143.
17. Fidai, S., S. B. Hinchigeri, and W. R. Richards. 1994. Association of protochlorophyllide with the PufQ protein of Rb. capsulatus. Biochem. Biophys. Res. Commun. 200:1676-1684.
18. Fidai, S., S. B. Hinchigeri, R. J. Borgford, and W. R. Richards. 1994. Identification of the PufQ protein in membranes of Rhodobacter capsulatus. J. Bacteriol. 176:7244-7251.
19. Forrest, M. E., A. P. Zuccuni, and J. T. Beatty. 1989. The pufQ gene product of Rhodobacter capsulatus is essential for formation of B800-850 light-harvesting complexes. Curr. Microbiol. 19:123-127.
20. Garcia, A. F., G. Venturoli, N. Gad'on, J. G. Fernández-Velasco, B. A. Melandri, and G. Drews. 1987. The adaptation of the electron transfer chain of Rps. capsulata to different light intensities. Biochim. Biophys. Acta 890: 335-345.
21. Garcia, D., P. Richaud, J. Breton, and A. Vermeglio. 1994. Structure and function of the tetraheme cytochrome associated to the reaction center of Roseobacter denitrificans. Biochimie 76:666-673.
22. Gong, L., J. K. Lee, and S. Kaplan. 1994. The Q gene of Rhodobacter sphaeroides: its role in puf operon expression and spectral complex assembly. J. Bacteriol. 176:2946-2961.
23. Hanahan, D. 1985. Techniques for transformation of E. coli, p. 109-135. In D. M. Glover et al. (ed.), DNA cloning, vol. I. IRL Press, Oxford, England.
24. Harashima, K., and R. Kikuchi. 1988. Obligatory requirement of auxiliary oxidants for anaerobic phototrophic growth of Erythrobacter spec. OCh114, p. 147. In Abstracts of the VI International Symposium on Phototrophic Prokaryotes, Nordwijker Hout, The Netherlands.
25. Harashima, K., M. Nakagama, and N. Murata. 1982. Photochemical activities of bacteriochlorophyll in aerobically grown cells of Erythrobacter spec. OCh114 and Erythrobacter longus (OCh101). Plant Cell Physiol. 23:185-193.
26. Harashima, K., K. Kawazoe, I. Yoshida, and H. Kamata. 1987. Light-stimulated aerobic growth of Erythrobacter spec. OCh114. Plant Cell Physiol. 28:365-374.
27. Harashima, K., T. Shiba, and N. Murata. 1989. Aerobic photosynthetic bacteria. Japan Scientific Societies Press, Tokyo, Japan, and Springer Publishers, Berlin, Germany.
28. Henikoff, S. 1984. Unidirectional digestion with exonuclease III creates targeted break points for DNA sequencing. Gene 28:351-359.
29. Kaufmann, N., H. Hüdig, and G. Drews. 1984. Transposon Tn5 mutagenesis of genes for the photosynthetic apparatus in Rhodopseudomonas capsulatus. Mol. Gen. Genet. 198:153-158.
30. Klug, G. 1995. Post-transcriptional control of photosynthesis gene expression, p. 1235-1244. In R. E. Blankenship, M. T. Madigan, and C. E. Bauer (ed.), Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
31. Klug, G. Personal communication.
32. Klug, G., and S. N. Cohen. 1988. Pleiotropic effects of localized Rhodobacter capsulatus puf operon deletions on production of light-absorbing pigment-protein complexes. J. Bacteriol. 170:5814-5821.
33. Klug, G., and S. N. Cohen. 1991. Effects of translation on degradation of mRNA segments transcribed from polycistronic puf operon of Rhodobacter capsulatus. J. Bacteriol. 173:1478-1484.
34. Kortlüke, C. M. 1989. Die Genregion der membrangebundenen Hydrogenase von Alcaligenes eutrophus ist Bestandteil eines Megaplasmid-lokalisierten, Lithautotrophie-Gen clusters. Ph.D. thesis. Free University Berlin, Berlin, Germany.
35. Kortlüke, C. M., and G. Drews. Unpublished data.
36. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydrophobic character of a protein. J. Mol. Biol. 157:105-132.
37. Liebetanz, R., U. Hornberger, and G. Drews. 1991. Organization of the genes coding for the reaction center L and M subunits and B870 antenna polypeptides α and β from the aerobic photosynthetic bacterium Erythrobacter spec. OCh114. Mol. Microbiol. 5:1459-1468.
38. Lilburn, T. G., C. E. Haith, R. C. Prince, and J. T. Beatty. 1992. Pleiotropic effects of pufX gene deletion on the structure and function of the photosynthetic apparatus of Rhodobacter capsulatus. Biochim. Biophys. Acta 1100: 160-170.
39. Lilburn, T. G., R. C. Prince, and J. T. Beatty. 1995. Mutation of the Ser2 codon of the light-harvesting B870 α polypeptide of Rhodobacter capsulatus partially suppresses the pufX phenotype. J. Bacteriol. 177:4593-4600.
40. Marmur, J. 1961. A procedure for the isolation of deoxyribonucleic acids from microorganisms. J. Mol. Biol. 3:208-218.
41. Meryandini, A., and G. Drews. 1996. Import and assembly of the α- and β-polypeptides of the light-harvesting complex I (B870) in the membrane system of Rhodobacter capsulatus investigated in an in vitro translation system. Photosyn. Res. 47:21-31.
42. Nagashima, K. V. P., K. Matsuura, S. Ohyama, and K. Shimada. 1994. Primary structure and transcription of genes encoding B870 and photosynthetic reaction center apoprotein from Rubrivivax gelatinosus. J. Biol. Chem. 269:2477-2484.
43. Nagashima, K. V. P., K. Matsuura, and K. Shimada. 1996. The nucleotide sequence of the puf operon from the purple photosynthetic bacterium, Rhodospirillum molischianum: comparative analyses of light-harvesting proteins and the cytochrome subunits associated with the reaction centers. Photosyn. Res. 50:61-70.
44. Nishimura, K., H. Shimada, H. Ohta, T. Masuda, Y. Shioi, and K. Takamiya. 1996. Expression of the puf operon in an aerobic photosynthetic bacterium, Roseobacter denitrificans. Plant Cell Physiol. 37:153-159.
45. Nitschke, W., and S. M. Dracheva. 1995. Reaction center associated cytochromes, p. 775-805. In R. E. Blankenship, M. T. Madigan, and C. E. Bauer (ed.), Anoxygenic photosynthetic bacteria. Kluwer Academic Publishers, Dordrecht, The Netherlands.
46. Okamura, K., K. Takamiya, and M. Nishimura. 1985. Photosynthetic electron transfer system is inoperative in anaerobic cells of Erythrobacter spec. strain OCh114. Arch. Microbiol. 142:12-17.
47. Okamura, K., F. Mitsumori, O. Ito, K. Takamiya, and M. Nishimura. 1986. Photophosphorylation and oxidative phosphorylation in intact cells and chromatophores of an aerobic, photosynthetic bacterium Erythrobacter sp. strain OCh114. J. Bacteriol. 168:1142-1146.
48. Pollock, D., C. E. Bauer, and P. A. Scolnick. 1988. Transcription of the Rhodobacter capsulatus nifHDK operon is modulated by the nitrogen source. Construction of plasmid expression vectors based on the nifHDK promoter. Gene 65:269-275.
49. Porra, R. J., W. Schäfer, N. Gad'on, I. Katheder, G. Drews, and H. Scheer. 1996. Origin of the two carbonyl oxygens of bacteriochlorophyll a: demonstration of two different pathways for the formation of ring E in Rhodobacter sphaeroides and Roseobacter denitrificans and of a common hydratase mechanism for 3-acetyl group formation. Eur. J. Biochem. 239:85-92.
50. Rao, M. J. K., and P. Argos. 1986. A conformational preference parameter to predict helices in integral membrane proteins. Biochim. Biophys. Acta 869:197-214.
51. Reidl, H., J. R. Golecki, and G. Drews. 1983. Energetic aspects of photophosphorylation capacity and reaction center content of Rhodopseudomonas capsulata, grown in a turbidostat under different irradiances. Biochim. Biophys. Acta 725:455-463.
52. Richter, P., and G. Drews. 1991. Incorporation of light-harvesting complex I α and β polypeptides into the intracytoplasmic membrane of Rhodobacter capsulatus. J. Bacteriol. 173:5336-5345.
53. Russel, M., and P. Model. 1984. Replacement of fip gene of Escherichia coli by an inactive gene cloned on a plasmid. J. Bacteriol. 159:1034-1039.
54. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
55. Sanger, F., S. Micklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
56. Schägger, H., and G. von Jagow. 1987. Tricine-sodium dodecyl sulfate polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166:368-379.
57. Schmidhauser, T. J., and D. R. Helinski. 1985. Regions of broad-host-range plasmid RK2 involved in replication and stable maintenance in nine species of gram-negative bacteria. J. Bacteriol. 164:446-455.
58. Shiba, T. 1991. Roseobacter litoralis gen. nov., sp. nov., and Roseobacter denitrificans sp. nov., aerobic pink-pigmented bacteria which contain bacteriochlorophyll a. Syst. Appl. Microbiol. 14:140-145.
59. Shioi, Y. 1986. Growth characteristics and substrate specificity of aerobic photosynthetic bacterium, Erythrobacter sp. OCh114. Plant Cell Physiol. 27: 567-572.
60. Simon, R., U. Priefer, and A. Pühler. 1983. Vector plasmids for in-vivo and in-vitro manipulations of gram-negative bacteria, p. 99. In A. Pühler (ed.), Molecular biology of bacteria-plant interaction. Springer Publishers, Berlin, Germany.
61. Stackebrandt, E., F. A. Rainey, and N. Ward-Rainey. 1996. Anoxygenic phototrophy across the phylogenetic spectrum: current understanding and future perspectives. Arch. Microbiol. 166:211-223.
62. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusion expression of specific genes. Proc. Natl. Acad. Sci. USA 82:1074-1078.
63. Takamiya, K., K. Iba, and K. Okamura. 1987. Reaction center complex from an aerobic photosynthetic bacterium Erythrobacter species OCh114. Biochim. Biophys. Acta 890:127-133.
64. Tichy, H.-V., K. U. Albien, N. Gad'on, and G. Drews. 1991. Analysis of the Rhodobacter capsulatus puc operon: the pucC gene plays a central role in the regulation of LHII expression. EMBO J. 10:2949-2955.
65. Weyer, K. A., F. Lottspeich, H. Gruenberg, F. Lang, D. Oesterhelt, and H. Michel. 1987. Amino acid sequence of the cytochrome subunit of the photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J. 6:2197-2202.
66. Weyer, K. A., W. Schäfer, F. Lottspeich, and H. Michel. 1987. The cytochrome subunit of the photosynthetic reaction center from Rhodopseudomonas viridis is a lipoprotein. Biochemistry 26:2909-2914.
67. Woodcock, D. M., P. J. Crowther, J. Doherty, S. Jefferson, E. DeCruz, M. Noyer-Weidner, S. S. Smith, M. Z. Michael, and M. W. Graham. 1989. Quantitative evaluation of E. coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 17: 3469-3478.
68. Youvan, D. C., S. Ismail, and E. J. Bylina. 1985. Chromosomal deletion and plasmid complementation of the photosynthetic reaction center and light-harvesting genes from Rhodobacter capsulatus. Gene 38:10-30.
69. Youvan, D. C., E. J. Bylina, M. Alberti, H. Begusch, and J. E. Hearst. 1984. Nucleotide and deduced polypeptide sequences of the photosynthetic reaction center, B870 antenna and flanking polypeptides from Rhodobacter capsulatus. Cell 37:949-957.
70. Yurkov, V., E. Stackebrandt, A. Holmes, J. A. Fuerst, P. Hugenholtz, J. Golecki, N. Gad'on, V. M. Gorlenko, E. Kompantseva, and G. Drews. 1994. The phylogenetic positions of novel aerobic, bacteriochlorophyll a-containing bacteria and description of Roseococcus thiosulfatophilus gen. nov., sp. nov., Erythromicrobium ramosum gen. nov., sp. nov., and Erythrobacter litoralis sp. nov. Int. J. System. Bacteriol. 44:427-434.