Heme ci or cn of the Cytochrome b6f Complex, A Short Retrospective

Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 41)


The unexpected existence of heme ci (or cn) of cytochrome b6f complex was revealed to the scientific community in Spring 2003 at the Gordon Bioenergetics conference, taking place at Kimball Union Academy, NH, USA. The three-dimensional structures of the complex were published back-to-back by two independent groups in Fall 2003 (Kurisu et al. Science 302:1009–1014, 2003; Stroebel et al. Nature 426:413–418, 2003). Further information about the physico-chemical properties of this unusual heme was gathered in the following years. Here we shall re-examine early evidence for the presence of this unusual cytochrome, originally called G (Lavergne. Biochim Biophys Acta 725:25–33, 1983; Joliot and Joliot. Biochim Biophys Acta 933:319–333, 1988), which show the role that heme ci plays in electron transfer in the cytochrome b6f complex.


Heme Iron Redox Titration F40Y Mutant Photosynthetic Electron Flow Weak Electron Density 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



High-potential heme b


Low-potential heme b

Cyt b6f

Cytochrome b6f complex


Electrochromic shift


Midpoint redox potential


Ferredoxin-NADP+ reductase


Light Harvesting Complex 2


Nicotinamide adenine dinucleotide phosphate


2-n-nonyl-4-hydroxyquinoline N-oxide


Photosystem I


Photosystem II





We acknowledge Daniel Picot for stimulating discussion and help in drawing Fig. 15.5. Work in FZ laboratory was supported by Unité Mixte de Recherche 7099, CNRS, and Université Paris Diderot and by the “Initiative d’Excellence” program (Grant “DYNAMO,” ANR-11-LABX-0011-01).


  1. Adachi S, Nagano S, Ishimori K, Watanabe Y, Morishima I, Egawa T, Kitagawa T, Makino R (1993) Roles of proximal ligand in heme proteins: replacement of proximal histidine of human myoglobin with cysteine and tyrosine by site-directed mutagenesis as models for P-450, chloroperoxidase, and catalase. Biochemistry 32:241–252CrossRefPubMedGoogle Scholar
  2. 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 U S A 102:15860–15865CrossRefPubMedPubMedCentralGoogle Scholar
  3. Baymann F, Giusti F, Picot D, Nitschke W (2007) The c i/b H moiety in the b 6 f complex studied by EPR: a pair of strongly interacting hemes. Proc Natl Acad Sci U S A 104:519–524CrossRefPubMedPubMedCentralGoogle Scholar
  4. Berry EA, Huang LS, DeRose VJ (1991) Ubiquinol-cytochrome c oxidoreductase of higher plants. Isolation and characterization of the bc 1 complex from potato tuber mitochondria. J Biol Chem 266:9064–9077PubMedGoogle Scholar
  5. Cramer WA, Zhang H (2006) Consequences of the structure of the cytochrome b 6 f complex for its charge transfer pathways. Biochim Biophys Acta 1757:339–345CrossRefPubMedGoogle Scholar
  6. Das TK, Wilson EK, Cutruzzola F, Brunori M, Rousseau DL (2001) Binding of NO and CO to the d 1 heme of cd 1 nitrite reductase from Pseudomonas aeruginosa. Biochemistry 40:10774–10781CrossRefPubMedGoogle Scholar
  7. de Lacroix de Lavalette A, Barbagallo RP, Zito F (2008) Why is it so difficult to construct Qi site mutants in Chlamydomonas reinhardtii? Comptes Rendus Biol 331:510–517CrossRefGoogle Scholar
  8. de Lacroix de Lavalette A, Barucq L, Alric J, Rappaport F, Zito F (2009) Is the redox state of the c i heme of the cytochrome b 6 f complex dependent on the occupation and structure of the Qi site and vice versa? J Biol Chem 284:20822–20829CrossRefGoogle Scholar
  9. de Vitry C, Desbois A, Redeker V, Zito F, Wollman FA (2004) Biochemical and spectroscopic characterization of the covalent binding of heme to cytochrome b 6. Biochemistry 43:3956–3968CrossRefPubMedGoogle Scholar
  10. Duysens LNM (1954) Reversible changes in the absorption spectrum of chlorella upon irradiation. Science 120:353–354CrossRefPubMedGoogle Scholar
  11. Duysens LN (1956) The flattening of the absorption spectrum of suspensions, as compared to that of solutions. Biochim Biophys Acta 19:1–12CrossRefPubMedGoogle Scholar
  12. Furbacher PN, Girvin ME, Cramer WA (1989) On the question of interheme electron transfer in the chloroplast cytochrome b 6 in situ. Biochemistry 28:8990–8998CrossRefPubMedGoogle Scholar
  13. Hope AB, Rich PR (1989) Proton uptake by the chloroplast cytochrome bf complex. Biochim Biophys Acta 975:96–103CrossRefGoogle Scholar
  14. Huang D, Everly RM, Cheng RH, Heymann JB, Schagger H, Sled V, Ohnishi T, …, Cramer WA (1994) Characterization of the chloroplast cytochrome b 6 f complex as a structural and functional dimer. Biochemistry 33:4401–4409Google Scholar
  15. Joliot P, Joliot A (1988) The low-potential electron-transfer chain in the cytochrome b/f complex. Biochim Biophys Acta 933:319–333CrossRefGoogle Scholar
  16. Joliot P, Béal D, Frilley B (1980) A new spectrophotometric method for the study of photosynthetic reactions. J Chim Phys 77:209–216Google Scholar
  17. Jones RW, Whitmarsh J (1988) Inhibition of electron-transfer and the electrogenic reaction in the cytochrome b/f complex by 2-normal-nonyl-4-hydroxyquinoline N-oxide (NQNO) and 2,5-dibromo-3-methyl-6-isopropyl-P-benzoquinone (DBMIB). Biochim Biophys Acta 933:258–268CrossRefGoogle Scholar
  18. Kallas T (2012) Cytochrome b 6 f complex at the heart of energy transduction and redox signaling. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis. Springer, Dordrecht, pp 501–560CrossRefGoogle Scholar
  19. Kuras R, de Vitry C, Choquet Y, Girard-Bascou J, Culler D, Buschlen S, Merchant S, Wollman FA (1997) Molecular genetic identification of a pathway for heme binding to cytochrome b 6. J Biol Chem 272:32427–32435CrossRefPubMedGoogle Scholar
  20. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014CrossRefPubMedGoogle Scholar
  21. Lacambra M, Larsen U, Olive J, Bennoun P, Wollman FA (1984) Mutants of Chlorella sorokiniana: a new material for photosynthesis studies. I. Characterization of the thylakoid membranes of wild type and mutant strains. Photobiochem Photobiophys 8:191–205Google Scholar
  22. Lavergne J (1983) Membrane potential-dependent reduction of cytochrome b 6 in an algal mutant lacking photosystem-I centers. Biochim Biophys Acta 725:25–33CrossRefGoogle Scholar
  23. Lavergne J, Delosme R, Larsen U, Bennoun P (1984) Mutants of Chlorella sorokiniana: a new material for photosynthesis studies. II. Improved spectroscopic analysis of electron transfer in mutant strains. Photobiochem Photobiophys 8:207–219Google Scholar
  24. Liu Y, Moenne-Loccoz P, Hildebrand DP, Wilks A, Loehr TM, Mauk AG, Ortiz de Montellano PR (1999) Replacement of the proximal histidine iron ligand by a cysteine or tyrosine converts heme oxygenase to an oxidase. Biochemistry 38:3733–3743CrossRefPubMedGoogle Scholar
  25. Mitchell P (1975) The protonmotive Q-cycle: a general formulation. FEBS Lett 59:137–139CrossRefPubMedGoogle Scholar
  26. Mitchell P (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J Theor Biol 62:327–367CrossRefPubMedGoogle Scholar
  27. Pierre Y, Breyton C, Kramer D, Popot JL (1995) Purification and characterization of the cytochrome b 6 f complex from Chlamydomonas reinhardtii. J Biol Chem 270:29342–29349CrossRefPubMedGoogle Scholar
  28. Pierre Y, Breyton C, Lemoine Y, Robert B, Vernotte C, Popot JL (1997) On the presence and role of a molecule of chlorophyll a in the cytochrome b 6 f complex. J Biol Chem 272:21901–21908CrossRefPubMedGoogle Scholar
  29. Rappaport F, Finazzi G, Pierre Y, Bennoun P (1999) A new electrochemical gradient generator in thylakoid membranes of green algae. Biochemistry 38:2040–2047CrossRefPubMedGoogle Scholar
  30. Rich PR (1988) A critical-examination of the supposed variable proton stoichiometry of the chloroplast cytochrome-bf complex. Biochim Biophys Acta 932:33–42CrossRefGoogle Scholar
  31. Rich PR, Madgwick SA, Moss DA (1991) The interactions of duroquinol, dbmib and NQNO with the chloroplast cytochrome-bf complex. Biochim Biophys Acta 1058:312–328CrossRefGoogle Scholar
  32. Shihira I, Krauss RW (1965) Chlorella: Physiology and Taxonomy of Forty-one Isolates. University of Maryland, College ParkGoogle Scholar
  33. Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426:413–418CrossRefPubMedGoogle Scholar
  34. Whitelegge JP, Zhang H, Aguilera R, Taylor RM, Cramer WA (2002) Full subunit coverage liquid chromatography electrospray ionization mass spectrometry (LCMS+) of an oligomeric membrane protein: cytochrome b 6 f complex from spinach and the cyanobacterium Mastigocladus laminosus. Mol Cell Proteomics 1:816–827CrossRefPubMedGoogle Scholar
  35. Witt HT (1971) Coupling of quanta, electrons, fields, ions and phosphorylation in the functional membrane of photosynthesis. Results by pulse spectroscopic methods. Q Rev Biophys 4:365–477CrossRefPubMedGoogle Scholar
  36. 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 370:39–52CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  1. 1.Institut Biologie Physico-Chimique, UMR7099, CNRS/Université Paris DiderotParisFrance
  2. 2.IBEB/SBVME/LB3M Bât 161 CEA de CadaracheCedexFrance

Personalised recommendations