Abstract
The reaction between membrane-bound cytochrome c and the reaction center bacteriochlorophyll g dimer P798 was studied in the whole cells and isolated membranes of Heliobacterium gestii. In the whole cells, the flash-oxidized P798+ was rereduced in multiple exponential phases with half times (t 1/2s) of 10 μs, 300 μs and 4 ms in relative amplitudes of 40, 35 and 25%, respectively. The faster two phases were in parallel with the oxidation of cytochrome c. In isolated membranes, a significantly slow oxidation of the membrane-bound cytochrome c was detected with t 1/2 = 3 ms. This slow rate, however, again became faster with the addition of Mg2+. The rate showed a high temperature dependency giving apparent activation energies of 88.2 and 58.9 kJ/mol in the whole cells and isolated membranes, respectively. Therefore, membrane-bound cytochrome c donates electrons to the P798+ in a collisional reaction mode like the reaction of water-soluble proteins. The rereduction of the oxidized cytochrome c was suppressed by the addition of stigmatellin both in the whole cells and isolated membranes. This indicates that the electron transfer from the cytochrome bc complex to the photooxidized P798+ is mediated by the membrane-bound cytochrome c. The multiple flash excitation study showed that 2–3 hemes c were connected to the P798. By the heme staining after the SDS-PAGE analysis of the membraneous proteins, two cytochromes c were detected on the gel indicating apparent molecular masses of 17 and 30 kDa, respectively. The situation resembles the case in green sulfur bacteria, that is, the membrane-bound cyotochrome c z couples electron transfer between the cytochrome bc complex and the P840 reaction center complex.
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References
Albert I, Rutherford AW, Grav H, Kellermann J and Michel H (1998) The 18 kDa cytochrome c553 from Heliobacterium gestii: Gene sequence and characterization of the mature protein. Biochemistry 37: 9001–9008
Amesz J (1995) The Antenna-Reaction Center Complex of Heliobacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 687–697. Kluwer Academic Publishers, Dordrecht, The Netherlands
Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33: 91–111
Chiou H-C and Blankenship RE (1996) Temperature dependence of charge recombination in Heliobacillus mobilis. Photochem Photobiol 64: 32–37
Fuller RC, Sprague SG, Gest H and Blankenship RE (1985) A unique photosynthetic reaction center from Heliobacterium chlorum. FEBS Lett 182: 345–349
Hauska G, Hurt E, Gabellini N and Lockau L (1983) Comparative aspects of quinol-cytochrome c/plastocyanin oxidoreductases. Biochim Biophys Acta 726: 97–133
Hervás M, De la Rosa MA and Tollin G (1992) A comparative laser-flash absorption spectroscopy study of algal plastocyanin and cytochrome c552 photooxidation by Photosystem I particles from spinach. Eur J Biochem 203: 115–120
Hervás M, Navarro JA, Díaz A, Bottin H and De la Rosa MA (1995) Laser-flash kinetic analysis of the fast electron transfer from plastocyanin and cytochrome c6 to Photosystem I: Experimental evidence on the evolution of the reaction mechanism. Biochemistry 34: 11321–11326
Hope AB (2000) Electron transfers amongst cytochrome f, plastocyanin and Photosystem I: Kinetics and mechanisms. Biochim Biophys Acta 1456: 5–26
Itoh S (1979) Surface potential and reaction of membrane-bound electron transfer components. I. Reaction of P-700 in sonicated chloroplasts with redox reagents. Biochim Biophys Acta 548: 579–595.
Itoh S (1980) Effects of surface potential and membrane potential on the midpoint potential of cytochrome c-555 bound to the chromatophore membrane of Chromatium vinosum. Biochim Biophys Acta 591: 346–355.
IwakiM, Itoh S, Kamei S, Matsubara H and Oh-oka H (1999) Timeresolved spectroscopy of chlorophyll-a like electron acceptor in the reaction center complex of the green sulfur bacterium Chlorobium tepidum. Plant Cell Physiol 40: 1021–1028
Jenney FE, Prince RC and Daldal F (1994) Roles of the soluble cytochrome c2 and membrane-associated cytochrome cy of Rhodobacter capsulatus in photosynthetic electron transfer. Biochemistry 33: 2496–2502
Kleinherenbrink FAM and Amesz J (1993) Stoichiometries and rates of electron transfer and charge recombination in Heliobacterium chlorum. Biochim Biophys Acta 1143: 77–83
Kramer DM, Schoepp B, Liebl U and Nitschke W (1997) Cyclic electron transfer in Heliobacillus mobilis involving a menaquinol-oxidizing cytochrome bc complex and an RCI-type reaction center. Biochemistry 36: 4203–4211
Madigan MT (1992) The family Heliobacteria. In: Balows A, Trüper HG, Dworkin M and Schleifer K-H (eds) The Prokaryotes, second edition, pp 1981–1992. Springer-Verlag, New York
Madigan MT and Ormerod JG (1995) Taxonomy, Physiology and Ecology of Heliobacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 17–30. Kluwer Academic Publishers, Dordrecht, The Netherlands
Matsuura K, Masamoto K, Itoh S and Nishimura m (1980) Surface potential on the periplasmic side of the photosynthetic membrane of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 592: 121–129.
Meyer TE and Donohue TJ (1995) Cytochromes, iron-sulfur, and copper proteins mediating electron transfer from cyt bc1 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
Nitschke W, Liebl U, Matsuura K and Kramer DM (1995) Membrane-bound c-type cytochromes in Heliobacillus mobilis. In vivo study of the hemes involved in electron donation to the photosynthetic reaction center. Biochemistry 34: 11831–11839
Nitschke W, Schoepp B, Floss B, Schricker A, Rutherford AW and Liebl U (1996) Membrane-bound c-type cytochromes in Heliobacillus mobilis. Characterization by EPR and optical spectroscopy in membranes and detergent-solubilized material. Eur J Biochem 242: 695–702
Oh-oka H, Kamei S, Matsubara H, Iwaki M and Itoh S (1995) Two molecules of cytochrome c function as the electron donors to P840 in the reaction center complex isolated from a green sulfur bacterium, Chlorobium tepidum. FEBS Lett 365: 30–34
Oh-oka H, Iwaki M and Itoh S (1997) Viscosity dependence of the electron transfer rate from bound cytochrome c to P840 in the photosynthetic reaction center of the green sulfur bacterium Chlorobium tepidum. Biochemistry 36: 9267–9272
Oh-oka H, Iwaki M and Itoh S (1998) Membrane-bound cytochrome cz couples quinol oxidoreductase to the P840 reaction center complex in isolated membranes of the green sulfur bacterium Chlorobium tepidum. Biochemistry 37: 12293–12300
Okkels JS, Kjær B, Hansson Ö, Svendsen I, Møller, BL and Scheller HV (1992) A membrane-bound monoheme cytochrome c551 of a novel type is the immediate electron donor to P840 of the Chlorobium vibrioforme photosynthetic reaction center complex. J Biol Chem 267: 21139–21145
Ortega JM and Mathis P (1993) Electron transfer from the tetraheme cytochrome to the special pair in isolated reaction centers of Rhodopseudomonas viridis. Biochemistry 32: 1141–1151
Prince RC, Gest H and Blankenship RE (1985) Thermodynamic properties of the photochemical reaction center of Heliobacterium chlorum. Biochim Biophys Acta 810: 377–384
Schägger H, Link TA, Engel WD and von Jagow g (1986) Isolation of the eleven protein subunits of the bc1 complex from beef heart. Method Enzymol 126: 224–237
Smit HWJ, Amesz J and Van der Hoeven MFR (1987) Electron transport and triplet formation in membranes of the photosynthetic bacterium Heliobacterium chlorum. Biochim Biophys Acta 893: 232–240
Sone N, Tsuchiya N, Inoue M and Noguchi S (1996) Bacillus stearothermophilus qcr operon encoding Rieske FeS protein, cytochrome b6, and a novel-type cytochrome c1 of quinolcytochrome c reductase. J Biol Chem 271: 12457–12462
Tamura N, Itoh S, Yamamoto Y and Nishimura M (1981) Electrostatic interaction between plastocyanin and P700 in the electron transfer reaction of Photosystem I-enriched particles. Plant Cell Physiol 22: 603–612
Tamura N, Itoh S and Nishimura M (1983) Effects of net and local charges on the interaction between chemically-modified horse heart cytochrome c and P700 in Photosystem 1-enriched subchloroplast particles. Plant Cell Physiol 24: 215–223
Thomas PE, Ryan D and Levin W (1976) An improved staining procedure for the detection of the peroxidase activity of cytochrome P450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75: 168–176
Trost JT and Blankenship RE (1990) Isolation of a reaction center-particle and a small c-type cytochrome from Heliobacillus mobilis. In: Baltscheffsky M (ed) Current Research in Photosynthesis, pp 703–706. Kluwer Academic Publishers, Dordrecht, The Netherlands
Venturoli G, Mallardi A and Mathis P (1993) Electron transfer from cytochrome c2 to the primary donor of Rhodobacter sphaeroides reaction centers: A temperature dependence study. Biochemistry 32: 13245–13253
von Jagow G and Linik TA (1986) Use of specific inhibitors on the mitochondrial bc1 complex. Methods Enzymol 126: 253–271
Vos MH, Klaassen HE and Van Gorkom HJ (1989) Electron transport in Heliobacterium chlorum whole cells studied by electroluminescence and absorbance difference spectroscopy. Biochim Biophys Acta 973: 163–169
Woese CR, Debrunner-Vossbrinck BA, Oyaizu H, Stackebrandt E and Ludwig W (1985) Gram-positive bacteria: Possible photosynthetic ancestry. Science 229: 762–765
Xiong J, Inoue K and Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthetic gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95: 14851–14856
Xiong J, Fischer WM, Inoue K, Nakahara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730
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Oh-oka, H., Iwaki, M. & Itoh, S. Electron donation from membrane-bound cytochrome c to the photosynthetic reaction center in whole cells and isolated membranes of Heliobacterium gestii . Photosynthesis Research 71, 137–147 (2002). https://doi.org/10.1023/A:1014911832504
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DOI: https://doi.org/10.1023/A:1014911832504