Skip to main content
SpringerLink
Log in

Rieske/Cytochrome b Complexes: The Turbo Chargers of Chemiosmosis

  • Chapter
  • First Online:
The Structural Basis of Biological Energy Generation

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 39))

Summary

Rieske/cytochrome b complexes are transmembrane enzymes of many bioenergetic reaction chains. They operate according to a Q-cycle mechanism that allows the transfer of an extra proton over the membrane per electron transferred along the chain. Thus they optimize the ATP yield from the terminal electron donor/acceptor couples of the respective reaction chains. Two members of this family of enzymes, cytochrome bc 1 complex from proteobacteria and mitochondria and cytochrome b 6 f complex from cyanobacteria and chloroplast are well studied and crystal structures are available. While revealing unexpected features of the complexes, as the domain movement of the Rieske iron/sulfur protein and the presence of an unusual heme cofactor in a quinone binding pocket, they opened up new questions concerning the function of the enzyme. Few structural and functional studies are available for Rieske/cytb complexes from further species, which is the vast majority of bacterial and archeael phyla, and most information comes from genome analysis. Here we discuss structure and function of the complex from an evolutionary perspective.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

cytb :

– Cytochrome b;

DBMIB:

– 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone;

EPR:

– Electron Paramagnetic Resonance;

FNR:

– Ferredoxin NAD(P)H Reductase;

LUCA:

– Last Universal Common Ancestor;

NQNO:

– 2-n-nonyl-4-hydroxylquinoline N-oxide;

PS:

– Photosystem;

RC:

– Photosynthetic reaction center;

UHDBT:

– 5-n-undecyl-6-hydroxy-4,7-dioxobenzothiazole

References

  • Alric J, Pierre Y, Picot D, Lavergne J, Rappaport F (2005) Spectral and redox characterization of the heme c i of the cytochrome b 6 f complex. Proc Natl Acad Sci USA 102:15860–15865

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Anemüller S, Schäfer G (1990) Cytochrome aa3 from sulfolobus acidocaldarius. A single subunit, quinol-oxidizing archaebacterial terminal oxidase. Eur J Biochem 191:297–305

    Article  PubMed  Google Scholar 

  • Baymann F, Nitschke W (2010) Heliobacterial Rieske/cytb complex. Photosynth Res 104:177–187

    Article  CAS  PubMed  Google Scholar 

  • Baymann F, Lebrun E, Nitschke W (2004) Mitochondrial cytochrome c 1 is a collapsed di-heme cytochrome. Proc Natl Acad Sci 101:17737–17740

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baymann F, Giusti F, Picot D, Nitschke W (2007) The c i/b H-moiety in the cytochrome b 6 f complex studied by EPR. A pair of strongly interacting hemes. Proc Natl Acad Sci USA 104:519–524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brugna M, Nitschke W, Asso M, Guigliarelli B, Lemesle-Meunier D, Schmidt C (1998a) Redox components of cytochrome bc-type enzymes in acidophilic prokaryotes. II. The Rieske protein of phylogenetically distant acidophilic organisms. J Biol Chem 274:16766–16772

    Article  Google Scholar 

  • Brugna M, Albouy D, Nitschke W (1998b) Diversity of cytochrome bc complexes: example of the Rieske protein in green sulfur bacteria. J Bacteriol 180:3719–3723

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brugna M, Rodgers S, Schricker A, Montoya G, Kazmeier M, Nitschke W, Sinnig I (2000) A spectroscopic method for observing the domain movement of the Rieske iron-sulfur protein. Proc Natl Acad Sci USA 97:2069–2074

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brugna-Guiral M, Tron P, Nitschke W, Stetter KO, Burlat B, Guigliarelli B, Bruschi M, Giudici-Orticoni MT (2003) [NiFe] hydrogenases from the hyperthermophilic bacterium Aquifex aeolicus: properties, function, and phylogenetics. Extremophiles 7:145–157

    CAS  PubMed  Google Scholar 

  • Crofts AR, Meinhardt SW, Jones KR, Snozzi M (1983) The role of the quinone pool in the cyclic electron-transfer chain of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 723:202–218

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crofts AR, Shinkarev VP, Kolling DRJ, Hong S (2003) The modified Q-cycle explains the apparent mismatch between the kinetics of reduction of cytochrome c 1 and b H in the bc 1 complex. J Biol Chem 278:36191–36201

    Article  CAS  PubMed  Google Scholar 

  • Clark RD, Hind G (1983) Isolation of a five-polypeptide cytochrome b-f complex from spinach chloroplasts. J Biol Chem 258:10348–10354

    CAS  PubMed  Google Scholar 

  • Ducluzeau AL, Chenu E, Capowiez L, Baymann F (2008) The Rieske/cytochrome b complex of Heliobacteria. Biochim Biophys Acta 1777:1140–1146

    Article  CAS  PubMed  Google Scholar 

  • Ducluzeau AL, van Lis R, Duval S, Schoepp-Cothenet B, Russell MJ, Nitschke W (2009) Was nitric oxide the first deep electron sink? Trends Biochem Sci 34:9–15

    Article  CAS  PubMed  Google Scholar 

  • Esser L, Quinn B, Li YF, Zhang M, Elberry M, Yu L, Yu CA, Xia D (2004) Crystallographic studies of quinol oxidation site inhibitors: a modified classification of inhibitors for the cytochrome bc1 complex. J Mol Biol 341:281–302

    Article  CAS  PubMed  Google Scholar 

  • Glaser E, Dessi P (1999) Integration of the mitochondrial-processing peptidase into the cytochrome bc1 complex in plants. J Bioener Biomemb 31:259–274

    Article  CAS  Google Scholar 

  • Gray KA, Dutton PL, Daldal F (1994) Requirement of Histidine 217 for ubiquinol reductase activity (Qi site) in the cytochrome bc 1 complex. Biochemistry 33:723–733

    Article  CAS  PubMed  Google Scholar 

  • Hatefi Y, Haavik AG, Griffith DE (1962) Studies on the electron transfer system. J Biol Chem 237:1681–1685

    CAS  PubMed  Google Scholar 

  • Hill R (1954) The cytochrome b component of chloroplasts. Nature 4428:501–503

    Article  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1214

    Article  CAS  PubMed  Google Scholar 

  • Ingledew WJ (1982) Thiobacillus ferrooxidans. The bioenergetics of an acidophilic chemolithotroph. Biochim Biophys Acta 683:89–117

    Article  CAS  PubMed  Google Scholar 

  • Iwasaki T, Matsuura K, Oshima T (1995) Resolution of the aerobic respiratory system of the thermoacidophilic Archaeon, Sulfolobus sp. Strain 7. J Biol Chem 270:30881–30892

    Article  CAS  PubMed  Google Scholar 

  • Lebrun E, Santini JM, Brugna M, Ducluzeau AL, Ouchane S, Schoepp-Cothenet B, Baymann F, Nitschke W (2006) The Rieske protein; a case study on the pitfalls of multiple sequence alignments and phylogenetic reconstruction. Mol Biol Evol 23:1180–1191

    Article  CAS  PubMed  Google Scholar 

  • Komorowski L, Verheyen W, Schäfer G (2002) The Archaeal respiratory supercomplex SoxM from S. acidocaldarius combines features of quinol and cytochrome c oxidases. Biol Chem 383:1791–1799

    Article  CAS  PubMed  Google Scholar 

  • Kramer DM, Nitschke W, Cooley JW (2009) The cytochrome bc 1 and related bc complexes: Rieske/cytochrome b complexes as the functional core of a central electron/proton transfer complex. In: Hunter N, Daldal F, Thurnauer MC, Beatty JT (eds) The purple photosynthetic bacteria. Springer Science + Business Media BV, Dordrecht, pp 451–473

    Google Scholar 

  • Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014

    Article  CAS  PubMed  Google Scholar 

  • Malnoë A, Wollman FA, de Vitry C, Rappaport F (2011) Photosynthetic growth despite a broken Q-cycle. Nature Comm 2:301

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Espinosa RM, Dridge EJ, Bonete MJ, Butt JN, Butler CS, Sargent F, Richardson DJ (2007) Look on the positive side! The orientation, identification and bioenergetics of ‘Archaeal’ membrane-bound nitrate reductases. FEMS Microbiol Lett 276:129–139

    Article  CAS  PubMed  Google Scholar 

  • Miki T, Mikin M, Orii Y (1994) Membrane potential-linked reversed electron transfer in the beef heart cytochrome bc l complex reconstituted into potassium-loaded phospholipid vesicles. J Biol Chem 269:1827–1833

    CAS  PubMed  Google Scholar 

  • Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol 62:327–367

    Article  CAS  PubMed  Google Scholar 

  • Moret V, Pinamonti S, Fornasari E (1961) Polarographic study on the redox potential of ubiquinones. Biochim Biophys Acta 54:381–383

    Article  CAS  PubMed  Google Scholar 

  • Nelson N, Neumann J (1972) Isolation of a cytochrome b 6-f particle from chloroplasts. J Biol Chem 247:1817–1824

    CAS  PubMed  Google Scholar 

  • Okayama S (1976) Redox potential of plastoquinone A in spinach chloroplasts. Biochim Biophys Acta 440:331–336

    Article  PubMed  Google Scholar 

  • Rieske JS, Zaugg WS, Hansen RE (1964) Studies of the electron transfer system. LIX. Distribution of Iron and of the component giving an electron paramagnetic resonance signal at g = 1.90 in subfractions of complex III. J Biol Chem 239:3023–3030

    CAS  PubMed  Google Scholar 

  • Robertson DE, Prince RC, Bowyer JR, Matsuura K, Dutton L, Ohnishi T (1984) Thermodynamic properties of the semiquinone and its binding site in the ubiquinol-cytochrome c (c2) oxidoreductase of respiratory and photosynthetic systems. J Biol Chem 259:1758–1763

    CAS  PubMed  Google Scholar 

  • Schoepp B, Brugna M, Riedel A, Nitschke W, Kramer D (1999a) The Qo-site inhibitor DBMIB favours the proximal position of the chloroplast Rieske protein and induces a pK-shift of the redox linked proton. FEBS Lett 450:245–250

    Article  CAS  PubMed  Google Scholar 

  • Schoepp B, Brugna M, Lebrun E, Nitschke W (1999b) Iron-sulfur centers involved in photosynthetic light reactions. Adv Inorg Chem 47:335–360

    Article  CAS  Google Scholar 

  • Schütz M, Brugna M, Lebrun E, Baymann F, Huber R, Stetter KO, Hauska G, Toci R, Lemesle-Meunier D, Tron P, Schmidt C, Nitschke W (2000) Early evolution of cytochrome bc-complexes. J Mol Biol 300:663–676

    Article  PubMed  Google Scholar 

  • Schütz M, Schoepp-Cothenet B, Lojou E, Woudstra M, Lexa D, Tron P, Dolla A, Durand MC, Stetter KO, Baymann F (2003) The naphthoquinol oxidizing cytochrome bc 1 complex of the hyperthermophilic Knallgasbacterium Aquifex aeolicus: properties and phylogenetic relationships. Biochemistry 42:10800–10808

    Article  PubMed  Google Scholar 

  • Sone N, Fujiwara Y (1991) Effects of aeration during growth of Bacillus stearothermophilus on proton pumping activity and change of terminal oxidases. J Biochem 110:1016–1021

    CAS  PubMed  Google Scholar 

  • Sone N, Nagata K, Kojima H, Tajima J, Kodera Y, Kanamaru T, Noguchi S, Sakamoto S (2001) A novel hydrophobic diheme c-type cytochrome. Purification from Corynebacterium glutamicum and analysis of the QcrCBA operon encoding three subunit proteins of a putative cytochrome reductase complex. Biochim Biophys Acta 1503:279–290

    Article  CAS  PubMed  Google Scholar 

  • Sone N, Fukuda M, Katayama S, Jyoudai A, Syugyou M, Nogguchi S, Sakamoto J (2003) QcrCAB operon of a nocardia-form actinomyces Rhodococcus rhodochorus encodes cytochrome reductase complex with diheme cytochrome cc subunit. Biochim Biophys Acta 1557:125–131

    Article  CAS  PubMed  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418

    Article  CAS  PubMed  Google Scholar 

  • Swierczek M, Cieluch E, Sarewicz M, Borek A, Moser CC, Dutton PL, Osyczka A (2010) An electronic bus bar lies in the core of cytochrome bc 1. Science 329:451–454

    Article  CAS  PubMed  Google Scholar 

  • Tanaka T, Inoue M, Sakamoto J, Sone N (1996) Intra- and inter-complex cross-linking of subunits in the quinol oxidase super-complex from thermophilic Bacillus PS3. J Biochem 119:482–486

    Article  CAS  PubMed  Google Scholar 

  • ten Brink F, Schoepp-Cothenet B, van Lis R, Nitschke W, Baymann F (2013) Multiple Rieske/cytb complexes in a single organism. Biochim Biophys Acta 1827:1392–1406

    Article  PubMed  Google Scholar 

  • Wagner GC, Kassner RJ, Kamen MD (1974) Redox potentials of certain Vitamins K: Implications for a role in sulfite reduction by obligately Anaerobic Bacteria. Proc Natl Acad Sci USA 71:253–256

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Widger WR, Cramer WA, Herrmann RG, Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b 6-f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci 81:674–678

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xia D, Yu CA, Kim H, Xia JZ, Kachurin AM, Zhang L, Yu L, Deisenhofer J (1997) Crystal structure of the cytochrome bc 1 complex from bovine heart mitochondria. Science 277:60–66

    Article  CAS  PubMed  Google Scholar 

  • Yamashita E, Zhang H, Cramer WA (2007) Structure of the cytochrome b 6 f complex: quinone analogue inhibitors as ligands of heme c n. J Mol Biol 370:39–52

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yu J, Le Brun N (1988) Studies of the cytochrome subunits of menaquinone: cytochrome c reductase (bc-complex) of Bacillus subtilis. Evidence for the covalent attachment of heme to the cytochrome b subunit. J Biol Chem 273:8860–8866

    Article  Google Scholar 

  • Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts A, Berry E, Kim SH (1998) Electron transfer by domain movement in cytochrome bc 1. Nature 392:677–684

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Primak A, Bowman MK, Kramer DM, Cramer WA (2004) Characterization of the high-spin heme x in the cytochrome b 6 f complex of oxygenic photosynthesis. Biochemistry 43:16329–16336

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

The authors thank Barbara Schoepp-Cothenet, Wolfgang Nitschke and Daniel Picot for careful reading of the manuscript and helpful discussions. They are grateful to Daniel Picot and David Stroebel for the structure coordinates of the b 6 f complex from Chlamydomonas reinhardtii in the presence of NQNO. Frauke Baymann and Felix ten Brink are supported by a grant from the French ‘Agence nationale de la recherche’ (ANR-10-BLAN-1506).

Author information

Authors and Affiliations

  1. Bioénergétique et Ingénierie des protéines, Unité mixte de récherche 7281, Fédération de récherche 3479, Centre National de la Récherche Scientifique/Aix-Marseille Université, 31, chemin Joseph Aiguier, 13009, Marseille, France

    Felix ten Brink & Frauke Baymann

Authors
  1. Felix ten Brink
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frauke Baymann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frauke Baymann .

Editor information

Editors and Affiliations

  1. Department of Biotechnology, Norwegian University of Science and Technology, Trondheim, Sør-Trøndelag Fylke, Norway

    Martin F. Hohmann-Marriott

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Brink, F.t., Baymann, F. (2014). Rieske/Cytochrome b Complexes: The Turbo Chargers of Chemiosmosis. In: Hohmann-Marriott, M. (eds) The Structural Basis of Biological Energy Generation. Advances in Photosynthesis and Respiration, vol 39. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-8742-0_8

Download citation

Publish with us

Policies and ethics

Search

Navigation