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On the role of cytochrome c8 in photosynthetic electron transfer of the purple non-sulfur bacterium Rhodoferax fermentans

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Abstract

We report on the isolation, purification and functional characterization of a soluble c-type cytochrome from light-grown cells of the purple phototroph Rhodoferax fermentans. This cytochrome is basic (pI = 8), has a molecular mass of 12 kDa, and is characterized by a midpoint reduction potential of +285 mV. Partial analysis of the N-terminus amino-acid sequence shows a high similarity with cytochromes of c8 type (formerly called Pseudomonas cytochrome c-551 type). Time-resolved spectrophotometric studies show that this cytochrome c8 reduces the tetraheme subunit of the photosynthetic reaction center, in a fast (sub-ms) and a slow (ms) phase. Competition experiments in the presence of both cytochrome c8 and high potential iron-sulfur protein (HiPIP), isolated from the same microorganism, show that cytochrome c8 oxidation is decreased upon addition of HiPIP. These observations suggest that cytochrome c8 and HiPIP might play alternative roles in the photosynthetic electron flow of Rhodoferax fermentans.

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References

  • Almassy RJ and Dickerson RE (1978) Pseudomonas cytochrome c-551 at 2.0 Å resolution: Enlargement of the cytochrome c family. Proc Natl Acad Sci USA 75: 2674–2678

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW and Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410

    Google Scholar 

  • Ambler RP (1973) Bacterial cytochromes c and molecular evolution. Syst Zool 22: 554–565

    Google Scholar 

  • Ambler RP (1991) Sequence variability in bacterial cytochromes c. Biochim Biophys Acta 1058: 42–47

    Google Scholar 

  • Ambler RP and Meyer TE (1979) Anomalies in amino acid sequences of small cytochromes c and cytochromes c' from two species of purple photosynthetic bacteria. Nature (London) 278: 661–662

    Google Scholar 

  • Ambler RP and Wynn M (1973) The amino acid sequences of cytochromes c-551 from three species of Pseudomonas. Biochem J 131: 485–498

    Google Scholar 

  • Bartsch RG (1971) Cytochromes: Bacterial. Methods Enzymol 23: 344–363

    Google Scholar 

  • Bartsch RG (1991) The distribution of soluble metallo-proteins in purple phototrophic bacteria. Biochim Biophys Acta 1058: 28–30

    Google Scholar 

  • Bertini I, Ciurli S and Luchinat C (1995) The electronic structure of FeS centers in proteins and models. A contribution to the understanding of their electron transfer properties. Struct Bonding 83: 1–53

    Google Scholar 

  • Blankenship RE, Madigan MT and Bauer CE (1995) Anoxygenic Photosynthetic Bacteria. Kluwer Academic Publishers, Dordrecht, the Netherlands

    Google Scholar 

  • Bowyer JR, Tierney GV and Crofts AR (1979) Cytochrome c2-reaction center coupling in chromatophores of Rhodopeudomonas sphaeroides and Rhodopseudomonas capsulata. FEBS Lett 101: 207–212

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248–254

    Google Scholar 

  • Caffrey MS, Bartsch RG and Cusanovich MA (1992) Study of cytochrome c 2-reaction center interaction by site-directed mutagenesis. J Mol Biol 267: 6317–6321

    Google Scholar 

  • Carter CW, Kraut J, Freer ST, Alden RA, Sieker LC, Adman E and Jensen LH (1972) A comparison of Fe4S4 clusters in high potential iron protein and in ferredoxin. Proc Natl Acad Sci USA 69: 3526–3529

    Google Scholar 

  • Dutton PL (1978) Redox potentiometry: determination of midpoint potentials of oxidation-reduction components of biological electron-transfer systems. Methods Enzymol 54: 411–435

    Google Scholar 

  • Dutton PL, Petty KM, Boner HS and Morse SD (1975) Cytochrome c 2 and reaction center of Rhodopseudomonas sphaeroides Ga membranes. Extinction coefficients, content, half-reduction potentials, kinetics and electric field alterations. Biochim Biophys Acta 387: 536–556

    Google Scholar 

  • Fujiwara T, Yamanaka T and Fukumori Y (1995) The amino acid sequence of Nitrosomonas europea cytochrome c-552. Curr Microbiol 31: 1–4

    Google Scholar 

  • Hirahishi A, Hoshino Y and Satoh T (1991) Rhodoferax fermentans gen. nov., sp. nov., a phototrophic purple non-sulfur bacterium previously referred to as the 'Rhodocyclus gelatinosus-like' group. Arch Microbiol 155: 330–336

    Google Scholar 

  • Hochkoeppler A, Ciurli S, Venturoli G and Zannoni D (1995a) The high-potential iron-sulfur protein (HiPIP) from Rhodoferax fermentans is competent in photosynthetic electron transfer. FEBS Lett 357: 70–74

    Google Scholar 

  • Hochkoeppler A, Kofod P, Ferro G and Ciurli S (1995b) Isolation, characterization and functional role of the high-potential iron-sulfur protein from Rhodoferax fermentans. Arch Biochem Biophys 322: 313–318

    Google Scholar 

  • Hochkoeppler A, Moschettini G and Zannoni D (1995c) The electron transport system of the facultative phototroph Rhodoferax fermentans. I. A functional, thermodynamic and spectroscopic study of the respiratory chain of dark-and light-grown cells. Biochim Biophys Acta 1229: 73–80

    Google Scholar 

  • Hochkoeppler A, Zannoni D and Venturoli G (1995d) The electron transport system of the facultative phototroph Rhodoferax fermentans. II. Flash-induced oxidation of membrane-bound cytochromes c. Biochim Biophys Acta 1229: 81–88

    Google Scholar 

  • Hochkoeppler A, Ciurli S, Zannoni D, Meyer TE, Cusanovich MA and Tollin G (1996) Kinetics of photoinduced electron transfer from high potential iron-sulfur protein (HiPIP) to the photosyn-thetic reaction center of the purple phototroph Rhodoferax fermentans. Proc Natl Acad Sci USA 93: 6998–7002

    Google Scholar 

  • Hreggvidsson GO (1991) Two structurally different cytochromes c from Bacillus azotoformans: On the evolution of gram-positive bacteria. Biochim Biophys Acta 1058: 52–55

    Google Scholar 

  • Kerfeld CA, Chan C, Hirazawa M, Kleis-SanFrancisco S, Yeates TO and Knaff DB (1996) Isolation and characterization of soluble electron transfer proteins from Chromatium purpuratum. Biochemistry 35: 7812–7818

    Google Scholar 

  • Knaff DB, Whestone R and Carr JW (1980) The role of soluble cytochrome c-551 in cyclic electron flow-driven active transport in Chromatium vinosun. Biochim Biophys Acta 590: 50–58

    Google Scholar 

  • Knaff DB, Willie A, Long JE, Kriauciunas A, Durham B and Millet F (1991) Reaction of cytochrome c 2 with photosynthetic reaction centers from Rhodopseudomonas viridis. Biochemistry 30: 1303–1310

    Google Scholar 

  • Mathis P (1994) Electron transfer beween cytochrome c 2 and the isolated reaction center of the purple bacterium Rhodobacter sphaeroides. Biochim Biophys Acta 1187: 177–180

    Google Scholar 

  • 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 Netherlands

    Google Scholar 

  • 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: 4719–4726

    Google Scholar 

  • Moore GR and Pettigrew GW (1990) Cytochrome c: Evolutionary, Structural and Physiological Aspects. Springer-Verlag, Berlin

    Google Scholar 

  • Overfield RE and Wraight CA (1980) Oxidation of cytochromes c and c 2 by bacterial photosynthetic reaction centers in phospholipid vesicles. I. Studies with neutral membranes. Biochemistry 19: 3322–3327

    Google Scholar 

  • Prince RC, Cogdell RJ and Crofts AR (1974) The photo-oxidation of horse heart cytochrome c and native cytochrome c 2 by reaction centers from Rhodopseudomonas sphaeroides R26. Biochim Biophys Acta 347: 1–13

    Google Scholar 

  • Sanbongi Y, Ishii M, Igarashi Y and Kodama T (1989) Amino acid sequence of cytochrome c-552 from a thermophilic hydrogenoxidizing bacterium Hydrogenobacter thermophilus. J Bacteriol 171: 65–69

    Google Scholar 

  • Sanbongi Y, Chung SY, Yokoyama K, Igarashi Y and Kodana T (1992) Thermostability of Pseudomonas hydrogenothermophila cytochrome c-552. Biosci Biotechnol Biochem 56: 990–991

    Google Scholar 

  • 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: 689–696

    Google Scholar 

  • Schoepp B, Parot P, Menin L, Gaillard J, Richaud P and Vermeglio 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: 11736–11742

    Google Scholar 

  • Shill DA and Wood PM (1984) A role for cytochrome c 2 in Rhodopseudomonas viridis. Biochim Biophys Acta 764: 1–7

    Google Scholar 

  • Tedro SM, Meyer TE and Kamen MD (1979) Primary structure of a high potential, four-iron-four-sulfur ferredoxin from the photosynthetic bacterium Rhodospirillum tenue. J Biol Chem 254: 1495–1500

    Google Scholar 

  • Van Grondelle R, Duysens LNM, van der Wel JA and van der Wal HN (1977) Function and properties of a soluble c-type cytochrome c-551 in secondary photosynthetic electron transport in whole cells of Chromatium vinosum as studied with flash spectroscopy. Biochim Biophys Acta 461: 188–201

    Google Scholar 

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Authors and Affiliations

  1. Department of Biology, University of Bologna, Via Irnerio 42, 40126, Bologna, Italy

    Alejandro Hochkoeppler, Giovanni Venturoli & Davide Zannoni

  2. Institute of Agricultural Chemistry, Viale Berti-Pichat 10, 40127, Bologna, Italy

    Stefano Ciurli

  3. Department of Life Sciences and Chemistry, Roskilde University, DK-4000, Roskilde, Denmark

    Pauli Kofod

Authors
  1. Alejandro Hochkoeppler
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  2. Stefano Ciurli
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  3. Pauli Kofod
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  4. Giovanni Venturoli
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  5. Davide Zannoni
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Hochkoeppler, A., Ciurli, S., Kofod, P. et al. On the role of cytochrome c8 in photosynthetic electron transfer of the purple non-sulfur bacterium Rhodoferax fermentans. Photosynthesis Research 53, 13–21 (1997). https://doi.org/10.1023/A:1005830003198

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