Advertisement

Photosynthesis Research

, Volume 59, Issue 1, pp 39–52 | Cite as

Genes encoding light-harvesting and reaction center proteins from Chromatium vinosum

  • Gary E. Corson
  • Kenji V. P. Nagashima
  • Katsumi Matsuura
  • Yumiko Sakuragi
  • Ruwanthi Wettasinghe
  • Hong Qin
  • Randy AllenEmail author
  • David B. Knaff
Article

Abstract

Sequencing of a 3.4 kb DNA fragment isolated from the photosynthetic purple sulfur bacterium Chromatium vinosum and of PCR products has resulted in identification of the Chr. vinosum pufL, pufM, and pufC genes, reading from the 5′ to the 3′ direction, and coding, respectively, for the L, M and cytochrome c subunits of the reaction center of this bacterium. Other PCR products have been used to obtain complete sequences for the pufB and pufA genes, located immediately upstream from pufL and encoding the apoproteins of two Chr. vinosum light- harvesting proteins. The 3′-portion of the bchZ gene, a gene that codes for a protein involved in the biosynthesis of bacteriochlorophyll, has been located immediately upstream from pufB. A second pufB gene, pufB2, has been located downstream from pufC, as has the 5′-portion of a second pufA gene, pufA2. The location of a second set of pufB and pufA genes, encoding light- harvesting proteins, downstream from pufC has not previously been reported for any photosynthetic bacterium. Translation of the gene sequences encoding these Chr. vinosum light-harvesting proteins reveals both similarities to and differences from the amino acid sequences, obtained from direct sequencing of the apoproteins, previously reported for Chr. vinosum light-harvesting proteins. Translation of these gene sequences, and of those for pufL, pufM and pufC, revealed significant homology, at the amino acid level, to the corresponding peptides of photosynthetic purple non-sulfur bacteria.

antenna proteins puf operon purple sulfur bacteria; reaction center 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alegria G and Dutton PL (1990) Spectroscopic and electrochemical resolution of the high potential hemes in the reaction center of Chromatium vinosum using oriented Langmuir-Blodgett films. Biophys J 57: W-Pos 607Google Scholar
  2. Alegria G and Dutton PL (1991) Langmuir-Blodgett monolayer films of the Rhodopseudomonas viridis reaction center: Determination of the order of the hemes in the cytochrome c subunit. Biochim Biophys Acta 1057: 258–272Google Scholar
  3. Ausubel FM, Brent R, Kingston R, Moore D, Smith JA, Seidman JG and Struhl K (1987) Current Protocols in Molecular Biology, 1st edition, pp 2.4.1–2.5.2. J. Wiley Interscience Press, New YorkGoogle Scholar
  4. Beatty JT (1995) Organization of photosynthesis gene transcripts. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 1209–1219. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  5. Bélanger G, Bérard J, Corriveau P and Gingras G. (1988) The structural genes coding for the L and m subunits of Rhodospirillum rubrum photoreaction center. J Biol Chem 263: 7632–7638Google Scholar
  6. Bose SK (1963) Media for anaerobic growth of photosynthetic bacteria. In: Gest H San Pietro A and Vernon LP (eds) Bacterial Photosynthesis, pp 501–510. Antioch Press, Yellow Springs, OHGoogle Scholar
  7. Brunisholz RA and Zuber H (1992) Structure, function and organization of antenna polypeptides and antenna complexes from the three families of Rhodospirillaneae. Eur J Photochem Photobiol 15: 113–140Google Scholar
  8. Deisenhofer J, Epp O, Sinning I and Michel H (1995) Crystallographic refinement at 2.3 Åresolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 246: 429–457Google Scholar
  9. Dracheva SM, Drachev LA, Konstantinov AA, Semenov AY, Skulachev VP, Arutjunjan AM, Shuvalov VA and Zaberezhnaya SM (1988) Electrogenic steps in the redox reactions catalyzed by photosynthetic reaction-centre complex from Rhodopseudomonas viridis. Eur J Biochem 171: 253–264Google Scholar
  10. Dracheva S, Williams JA, Van Driessche G, Van Beeumen JJ and Blankenship RE (1991) The primary structure of cytochrome c-554 from the green photosynthetic bacterium Chloroflexus aurantiacus. Biochemistry 30: 11451–11458Google Scholar
  11. Fathir I, Tanaka K, Yoza K, Kojima A, Kobayashi M, Wang Z-Y Lottspeich F and Nozawa T (1997) The genes coding for the L,M and cytochrome subunits of the reaction center from the thermophilic purple sulfur bacterium Chromatium tepidum. Photosynth Res 51: 71–82Google Scholar
  12. Fritzsch G, Buchanan S and Michel H (1989) Assignment of cytochrome hemes in crystallized reaction centers from Rhodopseudomonas viridis. Biochim Biophys Acta 977: 157–162Google Scholar
  13. Garcia D, Parot P and Verméglio A (1987) Purification and characterization of the photochemical reaction center from the thermophilic purple sulfur bacterium Chromatium tepidum. Biochim Biophys Acta 894: 379–385Google Scholar
  14. Gardiner AT, MacKenzie RC, Barrett SJ, Kaiser K and Cogdell RJ (1996) The purple photosynthetic bacterium Rhodopseudomonas acidophila contains multiple puc peripheral antenna complex (LH2) genes: Cloning and initial characterisation of four β/α pairs. Photosynth Res 49: 223–235Google Scholar
  15. Hiraishi A (1992) Direct automated sequencing of 16S rDNA amplified by polymerase chain reaction from bacterial cultures without DNA purification. Lett Appl Microbiol 15: 210–213Google Scholar
  16. Hochkoeppler A, Ciurli S, Venturoli G and Zannoni D (1995) The high potential iron-sulfur protein (HiPIP) from Rhodoferax fermentans is competent in photosynthetic electron transfer. FEBS Lett 357: 70–74Google Scholar
  17. Hochkoeppler A, Zannoni A, Ciurli S, Meyer TE, Cusanovich MA and Tollin G (1996) Kinetics of photo-induced electron transfer from high-potential iron-sulfur protein to the photosynthetic reaction center of the purple phototroph Rhodoferax fermentans. Proc Natl Acad Sci USA 93: 6998–7002Google Scholar
  18. Kerfeld CA, Yeates TO and Thornber JP (1994) Biochemical and spectroscopic characterization of the reaction center-LH1 complex and the carotenoid-containing B820 subunit of Chromatium purpuratum. Biochim Biophys Acta 1185: 193–202Google Scholar
  19. Kerfeld CA, Chan C, Hirasawa M, Kleis-SanFrancisco S, Yeates TO and Knaff DB (1996) Isolation and characterization of soluble electron transfer proteins from Chromatium purpuratum. Biochemistry 35: 7812–7818Google Scholar
  20. Kihara T and Chance B (1969) Cytochrome photooxidation at liquid nitrogen temperatures in photosynthetic bacteria. Biochim Biophys Acta 189: 116–124Google Scholar
  21. Kihara T and Dutton PL (1970) Light-induced reactions in photosynthetic bacteria. I. Reactions in whole cells and in cell-free extracts at liquid nitrogen temperatures. Biochim Biophys Acta 205: 196–204Google Scholar
  22. Knaff DB, and Buchanan BB (1975) Cytochrome b and photosynthetic bacteria. Biochim Biophys Acta 376: 549–560Google Scholar
  23. Knaff DB, Willie A, Long JE, Kriauciunas A, Durham B and Millett F (1991) The reaction of cytochrome c 2 with reaction centers from Rhodpseudomonas viridis. Biochemistry 30: 1304–1310Google Scholar
  24. Kortluke C, Breese K, Gad'on N, Labahn A and Drews G (1997) 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. J Bacteriol 179: 5247–5258Google Scholar
  25. Lancaster CRD, Ermler U and Michel H (1995) The structures of photosynthetic reaction centers from purple bacteria as revealed by x-ray crystallography. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 503–526. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  26. Liebetanz R, Hornberger U and Drews G (1991) Organization of the genes coding for the reaction-centre L and M subunits and B870 antenna polypeptides α and β from the aerobic photosynthetic bacterium Erythrobacter species OCH114. Mol Microbiol 5: 1459–1468Google Scholar
  27. Lin L and Thornber JP (1975) Isolation and partial purification of the photochemical reaction center of Chromatium vinosum (Strain D). Photochem Photobiol 22: 37–40Google Scholar
  28. Menin L, Gaillard J, Parot P, Schoepp B, Nitschke W and Verméglio A (1998) Role of HiPIP as electron donor to the RC-bound cytochrome in photosynthetic purple bacteria. Photosynth Res 55: 343–348Google Scholar
  29. Meyer TE and Donohue TJ (1995) Cytochromes, iron-sulfur and copper proteins mediating electron transfer from the cyt bc 1 complex to photosynthetic reaction center complexes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 725–745. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  30. Meyer TE, Bartsch RG, Cusanovich MA and Tollin G (1993) Kinetics of photooxidation of soluble cytochromes, HiPIP and azurin by the photosynthetic reaction center of the purple phototrophic bacterium Rhodopseudomonas viridis. Biochemistry 32: 4719–4726Google Scholar
  31. Michel H, Weyer KA, Gruenberg H, Dunger I, Oesterhelt D and Lottspeich F (1986) The ‘light’ and ‘medium’ subunits of the photosynthetic reaction centre from Rhodopseudomonas viridis: Isolation of the genes, nucleotide and amino acid sequences. EMBO J 5: 1149–1158Google Scholar
  32. Nagashima KVP, Shimada K and Matsuura K (1993) Phylogenetic analysis of photosynthetic genes of Rhodocyclus gelatinosus: Possibility of horizontal gene transfer in purple bacteria. Photosynth Res 36: 185–191Google Scholar
  33. Nagashima KVP, Matsuura K, Ohyama S and Shimada K (1994) Primary structure and transcription of genes encoding B870 and photosynthetic reaction center apoproteins from Rubrivivax gelatinosus. J Biol Chem 269: 2477–2484Google Scholar
  34. Nagashima KVP, Matsuura K and Shimada K (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. Photosynth Res 50: 61–70Google Scholar
  35. Nagashima KVP, Matsuura K, Wakao N, Hiraishi A and Shimada K (1997a) Nucleotide sequences of genes coding for photosynthetic reaction center and light-harvesting proteins of Acidiphilum rubrum and related aerobic acidophilic bacteria. Plant Cell Physiol 38: 1249–1258Google Scholar
  36. Nagashima KVP, Hiraishi A, Shimada K and Matsuura K (1997b) Horizontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J Mol Evol 45: 131–136Google Scholar
  37. Nagashima KVP, Sakuragi Y, Shimada K and Matsuura K (1998) Comparative analysis of the primary structure of the reaction center-bound cytochrome subunit in purple bacteria. Proceedings of the III Cadarache Conference on Reaction Centers, Photosynth Res (in press)Google Scholar
  38. Nitschke W and Rutherford AW (1989) Tetraheme cytochrome c subunit of Rhodpseudomonas viridis characterized by EPR. Biochemistry 28: 3161–3168Google Scholar
  39. Nitschke, W and Dracheva S (1995) Reaction center associated cytochromes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 775–805. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  40. Nitschke W, Jubault-Bregler M and Rutherford AW (1993) The reaction center associated tetraheme cytochrome subunit from Chromatium vinosum revisited: A reexamination of its EPR properties. Biochemistry 32: 8871–8879Google Scholar
  41. Nozawa T, Trost JT, Fukada T, Hatano M, McManus JD and Blankenship RE (1987) Properties of the reaction center of the thermophilic purple photosynthetic bacterium Chromatium tepidum. Biochim Biophys Acta 894: 468–476Google Scholar
  42. Okamura MY and Feher G (1995) Proton-coupled electron transfer reactions of QB in reaction centers from photosynthetic bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 577–594. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  43. Osyczka A, Nagashima KVP, Sogabe S, Miki K, Yoshida M, Shimada K and Matsuura K (1998) Interaction site for soluble cytochromes on the tetraheme cytochrome subunit bound to bacterial reaction center mapped by site directed mutagenesis. Biochemistry 37: 11732–11744Google Scholar
  44. Ovchinnikov YA, Abdulaev NG, Zolotarev AS, Shmukler BE. Zargarov AA, Kutuzov MA, Telezhinskaya IN and Levina NB (1988) Photosynthetic reaction centre of Chloroflexus aurantiacus. I. Primary structure of the L-subunit. FEBS Lett 231: 237–242Google Scholar
  45. Rao JKM and Argos P (1986) A conformational preference parameter to predict helices in integral membrane proteins. Biochim Biophys Acta 869: 197–214Google Scholar
  46. Samyn B, De Smet L, Van Driessche g, Meyer TE, Bartsch RG, Cusanovich MA and Van Beeumen JJ (1996) A high-potential soluble cytochrome c-551 from the purple phototrophic bacterium Chromatium vinosum is homologous to cytochrome c 8 from denitrifying pseudomonads. Eur J Biochem 236: 689–696Google Scholar
  47. Schoepp B, Parot P, Menin L, Gaillard J, Richaud P and Verméglio A (1995) In vivo participation of a high potential iron-sulfur protein as electron donor to the photochemical reaction center of Rubrivivax gelatinosus. Biochemistry 34: 11736–11742Google Scholar
  48. Shopes RJ, Levine LMA, Holten D and Wraight CA (1987) Kinetics of oxidation of the bound cytochromes in reaction centers from Rhodopseudomonas viridis. Photosynth Res 12: 165–180Google Scholar
  49. Tadros MH, Katsiou E, Hoon MA, Yurkova N and Ramij DP (1993) Cloning of a new antenna gene cluster and expression analysis of the antenna gene family of Rhodopseudomonas palustris. Eur J Biochem 217: 867–875Google Scholar
  50. Tiede DM, Leigh JS and Dutton PL (1978) Structural organization of the Chromatium vinosum reaction center associated c-cytochromes. Biochim Biophys Acta 503: 524–544Google Scholar
  51. Verméglio A, Richaud P and Breton J (1989) Orientation and assignment of the four cytochrome hemes in Rhodopseudomonas viridis reaction centers. FEBS Lett 243: 259–263Google Scholar
  52. Wagner-Huber R, Brunisholz RA, Bissig I, Frank G, Suter F and Zuber H (1992) The primary structure of the antenna polypeptides of Ectothiorhodospira halochloris and Ectothiorhodospira halophilla. Four core-type antenna polypeptides in Ec. halochloris and Ec. halophila. Eur J Biochem 205: 917–925Google Scholar
  53. Weyer KA, Lottspeich F, Gruenberg H, Lang F, Oesterhelt D and Michel H (1987a) Amino acid sequence of the cytochrome subunit of the photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J 8: 2197–2202Google Scholar
  54. Weyer KA, Schäfer W, Lottspeich F and Michel H (1987b) The cytochrome subunit of the photosynthetic reaction center from Rhodopseudomonas viridis is a lipoprotein. Biochemistry 26: 2909–2914Google Scholar
  55. Williams JC, Steiner LA, Ogden RC, Simon MI and Feher g (1983) Primary structure of the M subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 80: 6505–6509Google Scholar
  56. Williams JC, Steiner LA, Feher G and Simon MI (1984) Primary structure of the L subunit of the reaction center from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 81: 7303–7307Google Scholar
  57. Youvan DC, Bylina EJ, Alberti M, Begusch H and Hearst JE (1984) Nucleotide and deduced polypeptide sequences of the photosynthetic reaction center, B870 antenna and flanking polypeptides from R. capsulata. Cell 37: 949–957Google Scholar
  58. Zuber H and Cogdell RJ (1995) Structure and organization of purple bacterial antenna complexes. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 315–348. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  59. Zuker M and Stiegler P (1981) Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acid Res 9: 133–148Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Gary E. Corson
    • 1
  • Kenji V. P. Nagashima
    • 2
  • Katsumi Matsuura
    • 2
  • Yumiko Sakuragi
    • 2
  • Ruwanthi Wettasinghe
    • 3
  • Hong Qin
    • 1
  • Randy Allen
    • 3
    • 4
    Email author
  • David B. Knaff
    • 1
    • 3
  1. 1.Department of Chemistry and BiochemistryTexas Tech UniversityLubbockUSA
  2. 2.Department of BiologyTokyo Metropolitan UniversityTokyoJapan
  3. 3.Institute for BiotechnologyTexas Tech UniversityLubbockUSA
  4. 4.Departments of Biological Sciences and Plant and Soil SciencesTexas Tech UniversityLubbockUSA

Personalised recommendations