Skip to main content
SpringerLink
Log in

Discovery and characterization of electron transfer proteins in the photosynthetic bacteria

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Research on photosynthetic electron transfer closely parallels that of other electron transfer pathways and in many cases they overlap. Thus, the first bacterial cytochrome to be characterized, called cytochrome c 2, is commonly found in non-sulfur purple photosynthetic bacteria and is a close homolog of mitochondrial cytochrome c. The cytochrome bc 1 complex is an integral part of photosynthetic electron transfer yet, like cytochrome c 2, was first recognized as a respiratory component. Cytochromes c 2 mediate electron transfer between the cytochrome bc 1 complex and photosynthetic reaction centers and cytochrome a-type oxidases. Not all photosynthetic bacteria contain cytochrome c 2; instead it is thought that HiPIP, auracyanin, Halorhodospira cytochrome c551, Chlorobium cytochrome c555, and cytochrome c 8 may function in a similar manner as photosynthetic electron carriers between the cytochrome bc 1 complex and reaction centers. More often than not, the soluble or periplasmic mediators do not interact directly with the reaction center bacteriochlorophyll, but require the presence of membrane-bound intermediates: a tetraheme cytochrome c in purple bacteria and a monoheme cytochrome c in green bacteria. Cyclic electron transfer in photosynthesis requires that the redox potential of the system be delicately poised for optimum efficiency. In fact, lack of redox poise may be one of the defects in the aerobic phototrophic bacteria. Thus, large concentrations of cytochromes c 2 and c′ may additionally poise the redox potential of the cyclic photosystem of purple bacteria. Other cytochromes, such as flavocytochrome c (FCSD or SoxEF) and cytochrome c551 (SoxA), may feed electrons from sulfide, sulfur, and thiosulfate into the photosynthetic pathways via the same soluble carriers as are part of the cyclic system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

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

    Article  PubMed  CAS  Google Scholar 

  • Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987) Structure of the reaction center from Rhodobacter sphaeroides R-26: the protein subunits. Proc Natl Acad Sci USA 84: 6162–6166

    Article  PubMed  CAS  Google Scholar 

  • Almassy RJ and Dickerson RE (1978) Pseudomonas cytochrome c551 at 2.0 Å resolution: enlargement of the cytochrome c family. Proc Natl Acad Sci USA 75: 2674–2678

    Article  PubMed  CAS  Google Scholar 

  • Ambler RP (1963) The amino acid sequence of Pseudomonas cytochrome c551. Biochem J 89: 349–378

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ambler RP, Daniel M, Hermoso J, Meyer TE, Bartsch RG and Kamen MD (1979a) Cytochrome c2 sequence variation among the recognized species of purple non-sulfur photosynthetic bacteria. Nature (London) 278: 659–660

    Article  PubMed  CAS  Google Scholar 

  • from two species of purple photosynthetic bacteria}. Nature (London) 278: 661–662

    Article  PubMed  CAS  Google Scholar 

  • and c-556}. Proc Natl Acad Sci USA 78: 6854–6857

    Article  PubMed  CAS  Google Scholar 

  • Ambler RP, Daniel M, Melis K and Stout CD (1984) The amino acid sequence of the dihaem cytrochrome c4 from the bacterium Azotobacter vinelandii. Biochem J 222: 217–227

    PubMed  CAS  Google Scholar 

  • Ambler RP, Meyer TE and Kamen MD (1993) Amino acid sequences of cytochromes c-551 from the halophilic purple phototrophic bacteria Ectothiorhodospira halophila and E. halochloris. Arch Biochem Biophys 306: 83–93

    Article  PubMed  CAS  Google Scholar 

  • Appia-Ayme C, Little PJ, Matsumoto Y, Leech AP and Berks BC (2001) Cytochrome complex essential for photosynthetic oxidation of both thiosulfate and sulfide in Rhodovulum sulfidophilum. J Bacteriol 183: 6107–6118

    Article  PubMed  CAS  Google Scholar 

  • Arieli B, Shahak Y, Taglicht D, Hauska G and Padan E (1994) Purification and characterization of sulfide-quinone reductase, a novel enzyme driving anoxygenic photosynthesis in Oscillatoria limnetica. J Biol Chem 269: 5705–5711

    PubMed  CAS  Google Scholar 

  • Axelrod HL, Abresch EC, Okamura MY, Yeh AP, Rees DC and Feher G (2002) X-Ray structural determination of the cytochrome c2: reaction center electron transfer complex from Rhodobacter sphaeroides. J Mol Biol 319: 501–515

    Article  PubMed  CAS  Google Scholar 

  • Bamford BA, Bruno S, Rasmussen T, Appia-Ayme C, Cheesman MR, Berks BC and Hemmings AM (2002) Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme. EMBO J 21: 5599–5610

    Article  PubMed  CAS  Google Scholar 

  • Bartsch RG (1963) Nonheme iron proteins and Chromatium iron protein. In: Gest H, San Pietro A and Vernon LP (eds) Bacterial Photosynthesis, pp 315–326. Antioch Press, Yellow Springs, Ohio

    Google Scholar 

  • Bartsch RG and Kamen MD (1960) Isolation and properties of two soluble heme proteins in extracts of the photoanaerobe Chromatium. J Biol Chem 235: 825–831

    PubMed  CAS  Google Scholar 

  • Bersch B, Blackledge MJ, Meyer TE and Marion D (1996) Ectothiorhodospira halophila ferrocytochrome c551: NMR solution structure and comparison with bacterial cytochromes c. J Mol Biol 264: 567–584

    Article  PubMed  CAS  Google Scholar 

  • Bond CS, Blankenship RE, Freeman HC, Guss JM, Maher MJ, Selvaraj FM, Wilce MCJ and Willingham KM (2001) Crystal structure of auracyanin, a 'blue' copper protein from the green thermophilic photosynthetic bacterium Chloroflexus aurantiacus. J Mol Biol 306: 47–67

    Article  PubMed  CAS  Google Scholar 

  • Bronstein M, Schütz M, Hauska G, Padan E and Shahak Y (2000) Cyanobacterial sulfide-quinone reductase: cloning and heterologous expression. J Bacteriol 182: 3336–3344

    Article  PubMed  CAS  Google Scholar 

  • Bruce BD, Fuller RC and Blankenship RE (1982) Primary photochemistry in the facultatively aerobic green photosynthetic bacterium Chloroflexus aurantiacus. Proc Natl Acad Sci USA 79: 6532–6536

    Article  PubMed  CAS  Google Scholar 

  • Büttner B, Xie D-L, Nelson H, Pinther W, Hauska G and Nelson N (1992) Photosynthetic reaction center genes in green sulfur bacteria and in Photosystem 1 are related. Proc Natl Acad Sci USA 89:8135–8139

    Article  PubMed  Google Scholar 

  • Candela M, Zaccherini E and Zannoni D (2001) Respiratory electron transport and light-induced energy transduction in membranes from the aerobic photosynthetic bacterium Roseobacter denitrificans. Arch Microbiol 175: 168–177

    Article  PubMed  CAS  Google Scholar 

  • Carter DC, Melis KA, O'Donnell SE, Burgess BK, Furey WF Jr, Wang B-C and Stout CD (1985) Crystal structure of Azotobacter cytochrome c5 at 2.5 Å resolution. J Mol Biol 184: 279–295

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Koh M, Van Driessche G, Van Beeumen JJ, Bartsch RG, Meyer TE, Cusanovich MA and Mathews FS (1994) The structure of flavocytochrome c-sulfide dehydrogenase from the purple phototrophic bacterium, Chromatium vinosum. Science 266: 430–432

    Article  PubMed  CAS  Google Scholar 

  • Colbeau A, Kovacs KL, Chabert J and Vignais PM (1994) Cloning and sequencing of the structural genes (hupSLC) and accessory genes (hupDHI) for hydrogenase biosynthesis in Thiocapsa roseopersicina. Gene 140: 25–31

    Article  PubMed  CAS  Google Scholar 

  • Cusanovich MA and Bartsch RG (1969) A high potential cytochrome c from Chromatium chromatophores. Biochim Biophys Acta 189: 245–255

    Article  PubMed  CAS  Google Scholar 

  • Daldal F, Cheng S, Applebaum J, Davidson E and Prince RC (1986) Cytochrome c2 is not essential for photosynthetic growth of Rhodopseudomonas capsulata. Proc Natl Acad Sci USA 83: 2012–2016

    Article  PubMed  CAS  Google Scholar 

  • Davidson MW, Gray GO and Knaff DB (1985) Interaction of Chromatium vinosum flavocytochrome c-552 with cytochromes c studied by affinity chromatography. FEBS Lett 187: 155–159

    Article  CAS  Google Scholar 

  • Davidson MW, Meyer TE, Cusanovich MA and Knaff DB (1986) Complex formation between Chlorobium limicola f. thiosulfatophilum c-type cytochromes. Biochim Biophys Acta 850: 396–401

    Article  CAS  Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature (London) 318: 618–624

    Article  Google Scholar 

  • Dickerson RE, Takano T, Eisenberg D, Kallai OB, Samson L, Cooper A and Margoliash E (1971) Ferricytochrome c. 1. General features of the horse and bonito proteins at 2.8 Å resolution. J Biol Chem 246: 1511–1535

    PubMed  CAS  Google Scholar 

  • Dolata MM, Van Beeumen JJ, Ambler RP, Meyer TE and Cusanovich MA (1993) Nucleotide sequence of the flavocytochrome c heme subunit from the purple phototrophic bacterium, Chromatium vinosum. A 2.6 kilobase pair DNA fragment contains two multiheme cytochromes, a flavoprotein and a homolog of human ankyrin. J Biol Chem 268: 14426–14431

    PubMed  CAS  Google Scholar 

  • Donohue TJ, McEwan AG, Van Doren S, Crofts AR and Kaplan S (1988) Phenotypic and genetic characterization of cytochrome c2 deficient mutants of Rhodobacter sphaeroides. Biochemistry 27: 1918–1925

    Article  PubMed  CAS  Google Scholar 

  • Dracheva S, Williams JC, 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: 11451–11458

    Article  PubMed  CAS  Google Scholar 

  • Dus K, Sletten K and Kamen MD (1968) Cytochrome c2 of Rhodospirillum rubrum II. Complete amino acid sequence and phylogenetic relationships. J Biol Chem 243: 5507–5518

    PubMed  CAS  Google Scholar 

  • Eisen JA, Nelson KE, Paulsen IT, Heidelberg JF, Wu M, Dodson RJ, Deboy R, Gwinn ML, Nelson WC, Haft DH, Hickey EK, Peterson JD, Durkin AS, Kolonay JL, Yang F, Holt I, Umayam LA, Mason T, Brenner M, Shea TP, Parksey D, Nierman WC, Feldblyum TV, Hansen CL, Craven MB, Radune D, Vamathevan J, Khouri H, White O, Venter JC, Gruber TM, Ketchum KA, Tettelin H, Bryant DA and Fraser CM (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA 99: 9509–14.

    Article  PubMed  CAS  Google Scholar 

  • Errede B and Kamen MD (1978) Comparative kinetic studies of cytochromes c in reactions with mitochondrial cytochrome c oxidase and reductase. Biochemistry 17: 1015–1027

    Article  PubMed  CAS  Google Scholar 

  • from the photosynthetic purple sulfur bacterium, Chromatium vinosum}. Biochim Biophys Acta 1231: 220–222

    Article  PubMed  Google Scholar 

  • Feick RG, Fitzpatrick M and Fuller RC (1982) Isolation and characterization of cytoplasmic membranes and chlorosomes from the green bacterium Chloroflexus aurantiacus. J Bacteriol 150: 905–915

    PubMed  CAS  Google Scholar 

  • Fischer U (1988) Soluble electron-transfer proteins of Chlorobiaceae. In: Olson JM, Ormerod JG, Amesz J, Stackebrandt E and Trüper HG (eds) Green Photosynthetic Bacteria, pp 127–131. Plenum Press, New York

    Google Scholar 

  • Flory JE and Donohue TJ (1995) Organization and expression of the Rhodobacter sphaeroides cycFG operon. J Bacteriol 177: 4311–4320

    PubMed  CAS  Google Scholar 

  • Fowler CF, Nugent NA and Fuller RC (1971) The isolation and characterization of a photochemically active complex from Chloropseudomonas ethylica. Proc Natl Acad Sci USA 68: 2278–2282

    Article  PubMed  CAS  Google Scholar 

  • Freeman JC and Blankenship RE (1990) Isolation and characterization of the membrane-bound cytochrome c-554 from the thermophilic green photosynthetic bacterium Chloroflexus aurantiacus. Photosynth Res 23: 29–38

    Article  CAS  Google Scholar 

  • Friedrich CG (1998) Physiology and genetics of sulfur-oxidizing bacteria. Adv Microbial Physiol 39: 235–289.

    Article  CAS  Google Scholar 

  • Friedrich CG, Quentmeier A, Bardischewsky F, Rother D, Kraft R, Kostka S and Prinz H (2000) Novel genes coding for lithotrophic sulfur oxidation of Paracoccus pantotrophus. J Bacteriol 182: 4677–4687

    Article  PubMed  CAS  Google Scholar 

  • Friedrich CG, Rother D, Bardischewsky F, Quentmeier A and Fischer J (2001) Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism. Appl Environ Microbiol 67: 2873–2882

    Article  PubMed  CAS  Google Scholar 

  • Fukumori Y and Yamanaka T (1979a) Flavocytochrome c of Chromatium vinosum. Some enzymatic properties and subunit structure. J Biochem 85: 1405–1414

    PubMed  CAS  Google Scholar 

  • Fukumori Y and Yamanaka T (1979b) A high-potential nonheme iron protein (HiPIP)-linked, thiosulfate-oxidizing enzyme derived from Chromatium vinosum. Curr Microbiol 3: 117–120

    Article  CAS  Google Scholar 

  • Gabellini N and Sebald W (1986) Nucleotide sequence and transcription of the fbc operon from Rhodopseudomonas sphaeroides. Eur J Biochem 154: 569–579

    Article  PubMed  CAS  Google Scholar 

  • Gabellini N, Bowyer JR, Hurt E, Melandri BA and Hauska G (1982) A cytochrome b/c1 complex with ubiquinol-cytochrome c2 oxidoreductase activity from Rhodopseudomonas sphaeroides GA. Eur J Biochem 126: 105–111

    Article  PubMed  CAS  Google Scholar 

  • Gibson J (1961) Cytochrome pigments from the green photosynthetic bacterium Chlorobium thiosulphatophilum. Biochem J 79: 151–158

    PubMed  CAS  Google Scholar 

  • Haselkorn R, Lapidus A, Kogan Y, Vlcek C, Paces J, Paces V, Ulbrich P, Pecenkova T, Rebrekov D, Milgram A, M azur M, Cox R, K yrpides N, Ivanova N, K apatral V, Los T, Lykidis A, Mikhailova N, Reznik G, Vasieva O, Fonstein M (2001) The Rhodobacter capsulatus genome. Photosynth Res 70: 43–52.

    Article  PubMed  CAS  Google Scholar 

  • Hill R and Scarisbrick R (1951) The haematin compounds of leaves. New Phytol 50: 98–111

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hochkoeppler A, Zannoni D, 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: 6998–7002

    Article  PubMed  CAS  Google Scholar 

  • Horio T (1958a) Terminal oxidation system in bacteria. I. Purification of cytochromes from Pseudomonas aeruginosa. J Biochem 45: 195–205

    CAS  Google Scholar 

  • Horio T (1958b) Terminal oxidation system in bacteria II. Some physical and physiological properties of purified cytochromes of Pseudomonas aeruginosa. J Biochem 45: 267–279

    CAS  Google Scholar 

  • Horio T, Higashi T, Sasagawa M, Kusai K, Nakai M and Okunuki K (1960) Preparation of crystalline Pseudomonas cytochrome c-551 and its general properties. Biochem J 77: 194–201

    PubMed  CAS  Google Scholar 

  • Hurt EC and Hauska G (1984) Purification of membrane-bound cytochromes and a photoactive P840 protein complex of the green sulfur bacterium Chlorobium limicola f. thiosulfatophilum. FEBS Lett 168: 149–154

    Article  CAS  Google Scholar 

  • Jenney FE Jr, 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

    Article  PubMed  CAS  Google Scholar 

  • Kadziola A and Larsen S (1997) Crystal structure of the dihaem cytochrome c4 from Pseudomonas stutzeri determined at 2.2 Å resolution. Structure 5: 203–216

    Article  PubMed  CAS  Google Scholar 

  • Kamen MD and Takeda Y (1956) A comparative study of bacterial and mammalian cytochrome c. Biochim Biophys Acta 21: 518–523

    Article  PubMed  CAS  Google Scholar 

  • Kamen MD and Vernon LP (1954) Existence of haem compounds in a photosynthetic obligate anaerobe. J Bacteriol 67: 617–618

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Sato S, Kotani H,T anaka A, Azamizu E, N akamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, T akeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M and Tabata S (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3: 109–136

    Article  PubMed  CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Wolk CP Kuritz T, Sasamoto S, Watanabe A, Iriguchi M, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kohara M, Marsumoto M, Matsono A, Muraki A, Nakazaki N, Shimpo S, Sugimoto M, Takazawa M, Yamada M, Yasuda M and Tabata S (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8: 205–213

    Article  PubMed  CAS  Google Scholar 

  • Katoh S (1959) Studies on the algal cytochrome of c-type. J Biochem 46: 629–632

    Google Scholar 

  • Katoh S (1960) A new copper protein from Chlorella ellipsoidea. Nature (London) 186: 533–534

    Article  PubMed  CAS  Google Scholar 

  • Keilin D (1925) On cytochrome, a respiratory pigment, common to animals, yeast and higher plants. Proc R Acad Sci London Ser B 98: 312–339

    Article  Google Scholar 

  • Kennel SJ and Kamen MD (1971) Iron-containing proteins in Chromatium II. Purification and properties of cholate-solubilized cytochrome complex. Biochim Biophys Acta 234: 458–467

    Article  PubMed  CAS  Google Scholar 

  • Kennel SJ, Bartsch RG and Kamen MD (1972) Observations on light-induced oxidation reactions in the electron transfer system of Chromatium. Biophys J 12: 882–896

    Article  PubMed  CAS  Google Scholar 

  • Klarskov K, Verté F, Van Driessche G, Meyer TE, Cusanovich MA and Van Beeumen JJ (1998) The primary structure of soluble cytochrome c-551 from the phototrophic green sulfur bacterium, Chlorobium limicola. Biochemistry 37: 10555–10568

    Article  PubMed  CAS  Google Scholar 

  • Konig BW, Schilder LTM, Tervoort MJ and Van Gelder BF (1980) The isolation and purification of cytochrome c1 from bovine heart. Biochim Biophys Acta 621: 283–295

    PubMed  CAS  Google Scholar 

  • Kostanjevecki V, Brigé A, Meyer TE, Cusanovich MA and Van Beeumen JJ (2000) Sequence of the flavocytochrome c-sulfide dehydrogenase operon from the purple phototrophic bacterium, Ectothiorhodospira vacuolata. J Bacteriol 182: 3097–3103

    Article  PubMed  CAS  Google Scholar 

  • Kusai A and Yamanaka T (1973a) Cytochrome c553, Chlorobium thiosulfatophilum, is a sulfide cytochrome c reductase. FEBS Lett 34: 235–237

    Article  PubMed  CAS  Google Scholar 

  • Kusai A and Yamanaka T (1973b) The oxidation mechanisms of thiosulfate and sulfide in Chlorobium thiosulphatophilum: roles of cytochrome c-551 and cytochrome c-553. Biochim Biophys Acta 325: 304–314

    Article  PubMed  CAS  Google Scholar 

  • Kusai A and Yamanaka T (1973c) An NADP reductase derived from Chlorobium thiosulfatophilum: purification and some properties. Biochim Biophys Acta 292: 621–633

    Article  PubMed  CAS  Google Scholar 

  • Küsche WH and Trüper HG (1984) Cytochromes of the photosynthetic sulfur bacterium Ectothiorhodospira shaposhnikovii. Z Naturforsch 39c: 894–901

    Google Scholar 

  • Laycock MV (1972) The amino acid sequence of cytochrome c-553 from the chrysophycean alga Monochrysis lutheri. Can J Biochem 50: 1311–1325

    Article  PubMed  CAS  Google Scholar 

  • Lee WY, Brune DC, LoBrutto R and Blankenship RE (1995) Isolation, characterization, and primary structure of rubredoxin from the photosynthetic bacterium, Heliobacillus mobilis.Arch Biochem Biophys 318: 80–88

    Article  PubMed  CAS  Google Scholar 

  • Lovenberg W and Sobel BE (1965) Rubredoxin: a new electron transfer protein from Clostridium pasteurianum. Proc Natl Acad Sci USA 54: 193–199

    Article  PubMed  CAS  Google Scholar 

  • Mackenzie C, Choudhary M, Larimer FW, Predki PF, Stilwagen S, Armitage JP, Barber RD, Donohue TJ, Hosler JP, Newman JE, Shapleigh JP, Sockett RE, Zeilstra-Ryalls J and Kaplan S (2001) The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth Res 70: 19–41.

    Article  PubMed  CAS  Google Scholar 

  • MacMunn CA (1886) VI. Researches on myohaematin and the histohaematins. Phil Trans R Soc London 177: 267–298

    Article  Google Scholar 

  • Martinez SE, H uang D, Szczepaniak A, C ramer WA and Smith JL (1994) Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation. Structure 2: 95–105

    Article  PubMed  CAS  Google Scholar 

  • McManus JD, Brune DC, Han J, Sanders-Loehr J, Meyer TE, Cusanovich MA, Tollin G and Blankenship RE (1992) Isolation, characterization, and amino acid sequences of auracyanins, blue copper proteins from the green photosynthetic bacterium Chloroflexus aurantiacus. J Biol Chem 267: 6531–6540

    PubMed  CAS  Google Scholar 

  • Menin L, Schoepp B, Parot P and Verméglio A (1997) Photoinduced cyclic electron transfer in Rhodocyclus tenuis cells: participation of HiPIP or cyt c8 depending on the ambient redox potential. Biochemistry 36: 12183–12188

    Article  PubMed  CAS  Google Scholar 

  • Menin L, Gaillard J, Parot P, Schoepp B, Nitschke Wand Verméglio A (1998) Role of HiPIP as electron donor to the RC-bound cytochrome in photosynthetic purple bacteria. Photosynth Res 55: 343–348

    Article  CAS  Google Scholar 

  • Menin L, Yoshida M, Jaquinod M, Nagashima KVP, Matsuura K, Parot P and Verméglio A (1999) Dark aerobic growth conditions induce synthesis of a high midpoint potential cytochrome c8 in the photosynthetic bacterium Rubrivivax gelatinosus. Biochemistry 38: 15238–15244

    Article  PubMed  CAS  Google Scholar 

  • Merchant S and Bogorad L (1986) Regulation by copper of the expression of plastocyanin and cytochrome c552 in Chlamydomonas reinhardi. Mol Cell Biol 6: 462–469

    PubMed  CAS  Google Scholar 

  • Meyer TE (1985) Isolation and characterization of soluble cytochromes, ferredoxins, and other chromophoric proteins from the halophilic phototrophic bacterium, Ectothiorhodospira halophila. Biochim Biophys Acta 806: 175–183

    Article  PubMed  CAS  Google Scholar 

  • Meyer TE (1994) Purification and properties of high-potential iron- sulfur proteins. Method Enzymol 243: 435–447

    Article  CAS  Google Scholar 

  • Meyer TE (1996) Evolution and classification of c-type cytochromes. In: Scott RA and Mauk AG (eds) Cytochrome c. A Multidisciplinary Approach, pp 33–99. University Science Books, Sausalito, California

    Google Scholar 

  • Meyer TE and Bartsch RG (1976) The reaction of flavocytochrome c of the phototrophic sulfur bacteria with thiosulfate, sulfite, cyanide, and mercaptans. In: Singer TP (ed) Flavins and Flavoproteins, pp 312–317. Elsevier, Amsterdam

    Google Scholar 

  • Meyer TE and Kamen MD (1982) New perspectives on c-type cytochromes. Adv Prot Chem 35: 105–212

    Article  CAS  Google Scholar 

  • Meyer TE, Bartsch RG, Cusanovich MA and Mathewson JH (1968) The cytochromes of Chlorobium thiosulfatophilum. Biochim Biophys Acta 153: 854–861

    Article  PubMed  CAS  Google Scholar 

  • Meyer TE, Sharp JJ and Bartsch RG (1971) Isolation and properties of rubredoxin from the photosynthetic green sulfur bacteria. Biochim Biophys Acta 234: 266–269

    Article  PubMed  CAS  Google Scholar 

  • Meyer TE, Van Beeumen JJ, Ambler RP and Cusanovich MA (1997) The evolution of electron transfer proteins in phototrophic bacteria and denitrifying pseudomonads. In: Baltscheffsky H (ed.) Origin and Evolution of Biological Energy Conversion, pp 71–108. VCH Publishers, New York

    Google Scholar 

  • Mortenson LE, Valentine RC and Carnahan JE (1962) An electron transport factor from Clostridium pasteurianum. Biochem Biophys Res Comm 7: 448–452

    Article  PubMed  CAS  Google Scholar 

  • Nakamura Y, Kaneko T, Sato S, Ikeuchi M, Katoh H, Sasamoto S, Watanabe A, Iriguchi M, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M and Tabata S (2002) Complete Genome Structure of the Thermophilic Cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res. 9: 123–130.

    Article  PubMed  CAS  Google Scholar 

  • Ng TCN, Laheri AN and Maier RJ (1995) Cloning, sequencing, and mutagenesis of the cytochrome c4 gene from Azotobacter vinelandii: characterization of the mutant strain and a proposed new branch in the respiratory chain. Biochim Biophys Acta 1230: 119–129

    Article  PubMed  Google Scholar 

  • Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, Shukla HD, Lasky SR, Baliga NS, Thorsson V, Sbrogna J, Swartzell S, Weir D, Hall J, Dahl TA, Welti R, Goo YA, Leithauser B, Keller K, Cruz R, Danson MJ, Hough DW, Maddocks DG, Jablonski PE, Krebs MP, Angevine CM, Dale H, Isenbarger TA, Peck RF, Pohlschroder M, Spudich JL, Jung KW, Alam M, Freitas T, Hou S, Daniels CJ, Dennis PP, Omer AD, Ebhardt H, Lowe TM, Liang P, Riley M, Hood L and DasSarma S (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci U S A.97: 12176–81.

    Article  PubMed  CAS  Google Scholar 

  • Okkels JS, Kjær B, Hansson O, Svendsen I, Møller B 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

    PubMed  CAS  Google Scholar 

  • Olson JM and Chance B (1960a) Oxidation-reduction reactions in the photosynthetic bacterium Chromatium. 1. Absorption spectrum changes in whole cells. Arch Biochem Biophys 88: 26–39

    Article  PubMed  CAS  Google Scholar 

  • Olson JM and Chance B (1960b) Oxidation-reduction reactions in the photosynthetic bacterium Chromatium. 2. Dependence of light reactions on intensity of irradiation and quantum efficiency of cytochrome oxidation. Arch Biochem Biophys 88: 40–53

    Article  PubMed  CAS  Google Scholar 

  • Overfield RE, Wraight CA and Devault D (1979) Microsecond photooxidation kinetics of cytochrome c2 from Rhodopseudomonas sphaeroides: in vivo and solution studies. FEBS Lett 105: 137–142

    Article  PubMed  CAS  Google Scholar 

  • Parson WW and Case GD (1970) In Chromatium, a single photochemical reaction center oxidizes both cytochrome c552 and cytochrome c555. Biochim Biophys Acta 205: 232–245

    Article  PubMed  CAS  Google Scholar 

  • Pettigrew GW, Meyer TE, Bartsch RG and Kamen MD (1975) pH dependence of the oxidation-reduction potential of cytochrome c2. Biochim Biophys Acta 430: 197–208

    Google Scholar 

  • Pettigrew GW, Meyer TE, Bartsch RG and Kamen MD (1978) Redox potentials of the photosynthetic bacterial cytochromes c2and the structural bases for variability. Biochim Biophys Acta 503: 509–523

    Article  PubMed  CAS  Google Scholar 

  • Pierson BK and Thornber JP (1983) Isolation and spectral characterization of photochemical reaction centers from the thermophilic green bacterium Chloroflexus aurantiacus strain J-10–fl. Proc Natl Acad Sci USA 80: 80–84

    Article  PubMed  CAS  Google Scholar 

  • Prince RC and Olson JM (1976) Some thermodynamic and kinetic properties of the primary photochemical reactants in a complex from a green photosynthetic bacterium. Biochim Biophys Acta 423: 357–362

    Article  PubMed  CAS  Google Scholar 

  • Prince RC, Cogdell RJ and Crofts AR (1974) The photooxidation of horse heart cytochrome c and native cytochrome c2 by reaction centres from Rhodopseudomonas sphaeroides R26. Biochim Biophys Acta 347: 1–13

    Article  PubMed  CAS  Google Scholar 

  • Reinartz M, Tschäpe J, Brüser T, Trüper HG and Dahl C (1998) Sulfide oxidation in the phototrophic sulfur bacterium Chromatium vinosum. Arch Microbiol 170: 59–68

    Article  PubMed  CAS  Google Scholar 

  • Rey L and Maier RJ (1997) Cytochrome c terminal oxidase pathways of Azotobacter vinelandii: analysis of cytochrome c4and c5 mutants and up-regulation of cytochrome c-dependent pathways with N2 fixation. J Bacteriol 179: 7191–7196

    PubMed  CAS  Google Scholar 

  • Rickle GK and Cusanovich MA (1979) The kinetics of photooxidation of c-type cytochromes by Rhodospirillum rubrum reaction centers. Arch Biochem Biophys 197: 589–598

    Article  PubMed  CAS  Google Scholar 

  • Robinson NC and Talbert L (1980) Isolation of bovine cytochrome c1 as a single non-denatured subunit using gel filtration or high performance liquid chromatography in deoxycholate. Biochem Biophys Res Commun 95: 90–96

    Article  PubMed  CAS  Google Scholar 

  • Salemme FR, Freer ST, Xuong NH, Alden RA and Kraut J (1973) The structure of oxidized cytochrome c2 of Rhodospirillum rubrum. J Biol Chem 248: 3910–3921

    PubMed  CAS  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 c8from denitrifying pseudomonads. Eur J Biochem 236: 689–696

    Article  PubMed  CAS  Google Scholar 

  • Schatt E, Jouanneau Y and Vignais PM (1989) Molecular cloning and sequence analysis of the structural gene of ferredoxin I from the phototrophic bacterium, Rhodobacter capsulatus. J Bacteriol 171: 6218–6226

    PubMed  CAS  Google Scholar 

  • 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: 11736–11742

    Article  PubMed  CAS  Google Scholar 

  • Schütz M, Zirngibl S, le Coutre J, Büttner M, Xie D-L, Nelson N, Deutzmann R and Hauska G (1994) A transcription unit for the Rieske FeS-protein and cytochrome b in Chlorobium limicola. Photosynth Res 39: 163–174

    Article  Google Scholar 

  • Schütz M, Maldener I, Griesbeck C and Hauska G (1999) Sulfidequinone reductase from Rhodobacter capsulatus. Requirement for growth, peroplasmic location, and extension of gene sequence analysis. J Bacteriol 181: 6516–6523

    PubMed  Google Scholar 

  • Shahak Y, Schütz M, Bronstein M, Griesbeck C, Hauska G and Padan E (1999) Sulfide-dependent anoxygenic photosynthesis in prokaryotes. In: Peschek GA, Loffelhardt W and Schmetterer (eds) The Phototrophic Prokaryotes, pp 217–228. Kluwer Academic Publishers/Plenum Press, New York

    Google Scholar 

  • Shin M, Tagawa K and Arnon DI (1963) Crystallization of ferredoxin-TPN reductase and its role in the photosynthetic apparatus of chloroplasts. Biochem Z 338: 84–96

    PubMed  CAS  Google Scholar 

  • Shiozawa JA, Lottspeich F, O esterhelt D and Feick R (1989) The primary structure of the Chloroflexus aurantiacus reaction-center polypeptides. Eur J Biochem 180: 75–84

    Article  PubMed  CAS  Google Scholar 

  • Swank RT and Burris RH (1969) Purification and properties of cytochromes c of Azotobacter vinelandii. Biochim Biophys Acta 180: 473–489

    Article  PubMed  CAS  Google Scholar 

  • Tagawa K and Arnon DI (1962) Ferredoxins as electron carriers in photosynthesis and in the biological production and consumption of hydrogen gas. Nature (London) 195: 537–543

    Article  PubMed  CAS  Google Scholar 

  • Tedro SM, Meyer TE and Kamen MD (1976) Primary structure of a high potential iron-sulfur protein from the purple non-sulfur photosynthetic bacterium Rhodopseudomonas gelatinosa. J Biol Chem 251: 129–136

    PubMed  CAS  Google Scholar 

  • Tetreault M, Rongey SH, Feher G and Okamura MY (2001) Interaction between cytochrome c2 and the photosynthetic reaction center from Rhodobacter sphaeroides: effects of charge modification mutants on binding and electron transfer. Biochemistry 40: 8452–8462

    Article  PubMed  CAS  Google Scholar 

  • Tetreault M, Cusanovich M, Meyer T, Axelrod H and Okamura MY (2002) Double mutant studies identify electrostatic interactions that are important for docking cytochrome c2 onto the bacterial reaction center. Biochemistry 41: 5807–5815

    Article  PubMed  CAS  Google Scholar 

  • Then J and Trüper HG (1983) Sulfide oxidation in Ectothiorhodospira abdelmalekii. Evidence for the catalytic role of cytochrome c551. Arch Microbiol 135: 254–258

    Article  CAS  Google Scholar 

  • Then J and Trüper HG (1984) Utilization of sulfide and elemental sulfur by Ectothiorhodospira halochloris. Arch Microbiol 139: 295–298

    Article  CAS  Google Scholar 

  • Theorell H and Åkesson A (1939) Absorption spectrum of further purified cytochrome c. Science 90: 67

    Article  CAS  PubMed  Google Scholar 

  • Tissières A (1956) Purification, some properties and the specific biological activity of cytochromes c4 and c5 from Azotobacter vinelandii. Biochem J 64: 582–589

    PubMed  Google Scholar 

  • Trost JT, McManus JD, Freeman JC, Ramakrishna BL and Blankenship RE (1988) Auracyanin, a blue copper protein from the green photosynthetic bacterium Chloroflexus aurantiacus. Biochemistry 27: 7858–7863

    Article  CAS  Google Scholar 

  • Van Beeumen JJ (1991) Primary structure diversity of prokaryotic diheme cytochromes c. Biochim Biophys Acta 1058: 56–60

    Article  PubMed  CAS  Google Scholar 

  • Van Beeumen JJ, Ambler RP, Meyer TE, Kamen MD, Olson JM and Shaw EK (1976) The amino acid sequences of the cytochromes c-555 from two green sulfur bacteria of the genus Chlorobium. Biochem J 159: 757–774

    PubMed  CAS  Google Scholar 

  • Van Beeumen JJ, De Mol H, Samyn B, Bartsch RG, Meyer TE, Dolata MM and Cusanovich MA (1991) Covalent structure of the diheme cytochrome subunit and amino-terminal sequence of the flavoprotein subunit of flavocytochrome c from Chromatium vinosum. J Biol Chem 266: 12921–12931

    PubMed  CAS  Google Scholar 

  • Van Driessche G, Koh M, Chen ZW, Mathews FS, Meyer TE, Bartsch RG, Cusanovich MA and Van Beeumen JJ (1996) Primary structure of the flavoprotein subunit of the flavocytochrome c-sulfide dehydrogenase from the purple phototrophic bacterium Chromatium vinosum. Prot Sci 5: 1753–1764

    Article  CAS  Google Scholar 

  • Van Driessche G, Hu W, Van de Werken G, Selvariaj F, McManus J D, Blankenship RE and Van Beeumen JJ (1999) Auracyanin A from the thermophilic green gliding photosynthetic bacterium Chloroflexus aurantiacus represents an unusual class of small blue copper proteins. Prot Sci 8: 947–957

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Vernon LP (1953) Cytochrome c content of Rhodospirillum rubrum. Arch Biochem Biophys 43: 492–493

    Article  PubMed  CAS  Google Scholar 

  • Vernon LP and Kamen MD (1954) Hematin compounds in photosynthetic bacteria. J Biol Chem 211: 643–663

    PubMed  CAS  Google Scholar 

  • Verté F, Kostanjevecki V, De Smet L, Meyer TE, Cusanovich MA and Van Beeumen JJ (2002) Identification of a thiosulfate utilization gene cluster from the green phototrophic bacterium Chlorobium limicola. Biochemistry 41: 2932–2945

    Article  PubMed  CAS  Google Scholar 

  • Visser JM, de Jong GAH, Robertson LA and Kuenen JG (1997) A novel membrane-bound flavocytochrome c sulfide dehydrogenase from the colourless sulfur bacterium Thiobacillus sp.W5. Arch Microbiol 167: 295–301

    Article  PubMed  CAS  Google Scholar 

  • Wachtveitl J, Farchaus JW, Das R, Lutz M, Robert B and Mattioli TA (1993) Structure, spectroscopic, and redox properties of Rhodobacter sphaeroides reaction centers bearing point mutations near the primary electron donor. Biochemistry 32: 12875–12886

    Article  PubMed  CAS  Google Scholar 

  • : a dimeric, high-spin haem protein}. Nature (London) 286: 302–304

    Article  PubMed  CAS  Google Scholar 

  • Wood PM (1978) Interchangeable copper and iron proteins in algal photosynthesis, studies on plastocyanin and cytochrome c552 in Chlamydomonas. Eur J Biochem 87: 7–19

    Article  Google Scholar 

  • Wood PM (1980) Do photosynthetic bacteria contain cytochrome c1′ Biochem J 189: 385–391

    PubMed  CAS  Google Scholar 

  • Wood PM and Bendall DS (1975) The kinetics and spectroscopy of electron transfer from cytochromes and copper proteins to P700. Biochim Biophys Acta 387: 115–128

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, Inoue K and Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95: 14851–14856

    Article  PubMed  CAS  Google Scholar 

  • Yakushiji E (1935) Occurrence of cytochrome in higher plants and algae. Acta Phytochim (Japan) 8: 325–329

    CAS  Google Scholar 

  • Yakushiji E and Okunuki K (1940) New cytochrome component and its function. Proc Imp Acad (Tokyo) 16: 299–302

    Google Scholar 

  • Yamanaka T and Kusai A (1976) The function and some molecular features of cytochrome c-553 derived from Chlorobium thiosulfatophilum. In:Singer TP (ed) Flavins and Flavoproteins, pp 292–301. Elsevier, Amsterdam

    Google Scholar 

  • Yamanaka T and Okunuki K (1968) Comparative studies on reactivities of cytochrome c with cytochrome oxidases. In: Okunuki K, Sekuzu I and Kamen MD (eds) Structure and Function of Cytochromes, pp 390–403. University Park Press, Baltimore, Maryland

    Google Scholar 

  • Yoon KS, Hille R, Hemann C and Tabita FR (1999) Rubredoxin from the green suflur bacterium Chlorobium tepidum functions as an electron acceptor for pyruvate ferredoxin oxidoreductase. J Biol Chem 274: 29772–29778

    Article  PubMed  CAS  Google Scholar 

  • Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA and Kim SH (1998) Electron transfer by domain movement in cytochrome bc1. Nature (London) 392: 677–684

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, University of Arizona, Tucson, AZ, 85721, USA

    Terrance E. Meyer & Michael A. Cusanovich

Authors
  1. Terrance E. Meyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael A. Cusanovich
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Terrance E. Meyer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Meyer, T.E., Cusanovich, M.A. Discovery and characterization of electron transfer proteins in the photosynthetic bacteria. Photosynthesis Research 76, 111–126 (2003). https://doi.org/10.1023/A:1024910323089

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024910323089

Search

Navigation