Catalytic Reactions and Energy Conservation in the Cytochrome bc1 and b6f Complexes of Energy-Transducing Membranes

Sarewicz, Marcin; Pintscher, Sebastian; Pietras, Rafał; Borek, Arkadiusz; Bujnowicz, Łukasz; Hanke, Guy; Cramer, William A.; Finazzi, Giovanni; Osyczka, Artur

doi:10.1021/acs.chemrev.0c00712

Title: Catalytic Reactions and Energy Conservation in the Cytochrome bc₁ and b₆f Complexes of Energy-Transducing Membranes

Abstract

This review focuses on key components of respiratory and photosynthetic energy-transduction systems: the cytochrome bc₁ and b₆f (Cytbc₁/b₆ f) membranous multisubunit homodimeric complexes. These remarkable molecular machines catalyze electron transfer from membranous quinones to water-soluble electron carriers (such as cytochromes c or plastocyanin), coupling electron flow to proton translocation across the energy-transducing membrane and contributing to the generation of a transmembrane electrochemical potential gradient, which powers cellular metabolism in the majority of living organisms. Cytsbc₁/b₆ f share many similarities but also have significant differences. While decades of research have provided extensive knowledge on these enzymes, several important aspects of their molecular mechanisms remain to be elucidated. We summarize a broad range of structural, mechanistic, and physiological aspects required for function of Cytbc₁/b₆ f, combining textbook fundamentals with new intriguing concepts that have emerged from more recent studies. The discussion covers but is not limited to (i) mechanisms of energy-conserving bifurcation of electron pathway and energy-wasting superoxide generation at the quinol oxidation site, (ii) the mechanism by which semiquinone is stabilized at the quinone reduction site, (iii) interactions with substrates and specific inhibitors, (iv) intermonomer electron transfer and the role of a dimeric complex, and (v) higher levels of organizationmore »« less

Authors:

Sarewicz, Marcin ^[1];

^[1]; Pietras, Rafał ^[1]; Borek, Arkadiusz ^[1]; Bujnowicz, Łukasz ^[1]; Hanke, Guy ^[2]; Cramer, William A. ^[3]; Finazzi, Giovanni ^[4];

^[1]

Department of Molecular Biophysics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, 30-387 Kraków, Poland
School of Biological and Chemical Sciences, Queen Mary University of London, London E1 4NS, U.K.
Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907 United States
Laboratoire de Physiologie Cellulaire et Végétale, Université Grenoble Alpes, Centre National Recherche Scientifique, Commissariat Energie Atomique et Energies Alternatives, Institut National Recherche l’agriculture, l’alimentation et l’environnement, 38054 Grenoble Cedex 9, France

Publication Date:: Tue Jan 19 00:00:00 EST 2021

Research Org.:: Jagiellonian Univ., Krakow (Poland)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1767298

Alternate Identifier(s):: OSTI ID: 1767958

Grant/Contract Number:: SC0018238

Resource Type:: Published Article

Journal Name:: Chemical Reviews

Additional Journal Information:: Journal Name: Chemical Reviews Journal Volume: 121 Journal Issue: 4; Journal ID: ISSN 0009-2665

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

Subject:: 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; Redox reactions; Charge transfer; Bioinorganic chemistry; Peptides and proteins; Monomers

Citation Formats


                    Sarewicz, Marcin, Pintscher, Sebastian, Pietras, Rafał, Borek, Arkadiusz, Bujnowicz, Łukasz, Hanke, Guy, Cramer, William A., Finazzi, Giovanni, and Osyczka, Artur. Catalytic Reactions and Energy Conservation in the Cytochrome bc1 and b6f Complexes of Energy-Transducing Membranes.  United States: N. p., 2021. 
Web.  doi:10.1021/acs.chemrev.0c00712.

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                    Sarewicz, Marcin, Pintscher, Sebastian, Pietras, Rafał, Borek, Arkadiusz, Bujnowicz, Łukasz, Hanke, Guy, Cramer, William A., Finazzi, Giovanni, & Osyczka, Artur. Catalytic Reactions and Energy Conservation in the Cytochrome bc1 and b6f Complexes of Energy-Transducing Membranes.  United States.  https://doi.org/10.1021/acs.chemrev.0c00712

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                    Sarewicz, Marcin, Pintscher, Sebastian, Pietras, Rafał, Borek, Arkadiusz, Bujnowicz, Łukasz, Hanke, Guy, Cramer, William A., Finazzi, Giovanni, and Osyczka, Artur. Tue .  
"Catalytic Reactions and Energy Conservation in the Cytochrome bc1 and b6f Complexes of Energy-Transducing Membranes".  United States.  https://doi.org/10.1021/acs.chemrev.0c00712.

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@article{osti_1767298,

  title        = {Catalytic Reactions and Energy Conservation in the Cytochrome bc1 and b6f Complexes of Energy-Transducing Membranes},

  author       = {Sarewicz, Marcin and Pintscher, Sebastian and Pietras, Rafał and Borek, Arkadiusz and Bujnowicz, Łukasz and Hanke, Guy and Cramer, William A. and Finazzi, Giovanni and Osyczka, Artur},

  abstractNote = {This review focuses on key components of respiratory and photosynthetic energy-transduction systems: the cytochrome bc1 and b6 f (Cytbc1/b6 f) membranous multisubunit homodimeric complexes. These remarkable molecular machines catalyze electron transfer from membranous quinones to water-soluble electron carriers (such as cytochromes c or plastocyanin), coupling electron flow to proton translocation across the energy-transducing membrane and contributing to the generation of a transmembrane electrochemical potential gradient, which powers cellular metabolism in the majority of living organisms. Cytsbc1/b6 f share many similarities but also have significant differences. While decades of research have provided extensive knowledge on these enzymes, several important aspects of their molecular mechanisms remain to be elucidated. We summarize a broad range of structural, mechanistic, and physiological aspects required for function of Cytbc1/b6 f, combining textbook fundamentals with new intriguing concepts that have emerged from more recent studies. The discussion covers but is not limited to (i) mechanisms of energy-conserving bifurcation of electron pathway and energy-wasting superoxide generation at the quinol oxidation site, (ii) the mechanism by which semiquinone is stabilized at the quinone reduction site, (iii) interactions with substrates and specific inhibitors, (iv) intermonomer electron transfer and the role of a dimeric complex, and (v) higher levels of organization and regulation that involve Cytsbc1/b6 f. In addressing these topics, we point out existing uncertainties and controversies, which, as suggested, will drive further research in this field.},

  doi          = {10.1021/acs.chemrev.0c00712},

  journal      = {Chemical Reviews},

  number       = 4,

  volume       = 121,

  place        = {United States},

  year         = {Tue Jan 19 00:00:00 EST 2021},

  month        = {Tue Jan 19 00:00:00 EST 2021}

}

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Electrochemical and Spectroscopic Investigations of the Cytochrome bc 1 Complex from Rhodobacter capsulatus † journal, October 1999

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Reactions of the semiquinone free radicals of anti-tumour agents with oxygen and iron complexes journal, March 1985

Proton pump coupled to cytochrome c oxidase in mitochondria journal, March 1977

PGR5-PGRL1-Dependent Cyclic Electron Transport Modulates Linear Electron Transport Rate in Arabidopsis thaliana journal, February 2016

A semiquinone intermediate generated at the Qo site of the cytochrome bc1 complex: Importance for the Q-cycle and superoxide production journal, April 2007

A new concept for ferredoxin–NADP(H) oxidoreductase binding to plant thylakoids journal, November 2010

Transient inactivation of the thylakoid photosystem II light-harvesting protein kinase system and concomitant changes in intramembrane particle size during photoinhibition of Chlamydomonas reinhardtii. journal, July 1986

Stigmatellin. A dual type inhibitor of photosynthetic electron transport journal, May 1985

Interaction of positively charged amino acid residues of recombinant, cyanobacterial ferredoxin:NADP+ reductase with ferredoxin probed by site directed mutagenesis journal, January 1998

Modification of inhibitor binding sites in the cytochrome bf complex by directed mutagenesis of cytochrome b6 in Synechococcus sp. PCC 7002 journal, April 2001

Redox properties of the DBMIB-Rieske iron-sulfur complex in spinach chloroplast membranes journal, August 1981

Study of Inhibitory Effects and Action Mechanism of the Novel Fungicide Pyrimorph against Phytophthora capsici † journal, March 2010

The End of the Line: Can Ferredoxin and Ferredoxin NADP(H) Oxidoreductase Determine the Fate of Photosynthetic Electrons? journal, April 2014

An evolutionary analysis of the reaction mechanisms of photosystem I reduction by cytochrome c6 and plastocyanin journal, January 2002

The cyclic electron pathways around photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage journal, March 1994

Discovery of cytochrome bc 1 complex inhibitors inspired by the natural product karrikinolide journal, January 2016

Probing the Role of E272 in Quinol Oxidation of Mitochondrial Complex III † journal, August 2006

Loss of Phylloquinone in Chlamydomonas Affects Plastoquinone Pool Size and Photosystem II Synthesis journal, March 2007

The involvement of ferredoxin-NADP+ reductase in cyclic electron transport in chloroplasts journal, July 1981

Structural aspects of the cytochromeb 6 f complex; structure of the lumen-side domain of cytochromef journal, February 1994

Purification of highly active cytochrome bc1 complexes from phylogenetically diverse species by a single chromatographic procedure journal, May 1987

On the Mechanism of Quinol Oxidation in thebc1 Complex journal, August 1998

Protein−Protein Interactions between Cytochrome b and the Fe-S Protein Subunits during QH 2 Oxidation and Large-Scale Domain Movement in the bc 1 Complex † journal, February 2003

Intraprotein transfer of the quinone analogue inhibitor 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone in the cytochrome b6f complex journal, December 2005

The Q-cycle reviewed: How well does a monomeric mechanism of the bc1 complex account for the function of a dimeric complex? journal, July 2008

Association of Ferredoxin:NADP+ oxidoreductase with the photosynthetic apparatus modulates electron transfer in Chlamydomonas reinhardtii journal, June 2017

On the Redox Potentials of Ubiquinone and Cytochrome b in the Respiratory Chain journal, July 1969

Design of anti-parasitic and anti-fungal hydroxy-naphthoquinones that are less susceptible to drug resistance journal, May 2011

AS2077715 is a selective inhibitor of fungal mitochondrial cytochrome bc1 complex journal, May 2014

The Modified Q-cycle Explains the Apparent Mismatch between the Kinetics of Reduction of Cytochromes c 1 and b H in the bc 1 Complex journal, June 2003

Antimalarial 4(1H)-pyridones bind to the Q i site of cytochrome bc 1 journal, January 2015

Membrane-Anchored Cytochrome c y Mediated Microsecond Time Range Electron Transfer from the Cytochrome bc 1 Complex to the Reaction Center in Rhodobacter c apsulatus † journal, April 1998

UK-2A, B, C and D, Novel Antifungal Antibiotics from Streptomyces sp. 517-02. V. Inhibition Mechanism of Bovine Heart Mitochondrial Cytochrome bc1 by the Novel Antibiotic UK-2A. journal, January 1999

Role of Chloroplast Protein Kinase Stt7 in LHCII Phosphorylation and State Transition in Chlamydomonas journal, March 2003

Divergent pathways of photosynthetic electron transfer: The autonomous oxygenic and anoxygenic photosystems journal, November 1995

Molecular Quantum Dot Cellular Automata Based on Diboryl Monoradical Anions journal, January 2018

Myxothiazol, a new inhibitor of the cytochrome b-c1 segment of the respiratory chain journal, December 1981

Distance metrics for heme protein electron tunneling journal, July 2008

The reaction domain on Rhodospirillum rubrum cytochrome c2 and horse cytochrome c for the Rhodospirillum rubrum cytochrome bc1 complex. journal, October 1987

Single catalytic site model for the oxidation of ferrocytochrome c by mitochondrial cytochrome c oxidase. journal, January 1984

Complete Structure of the 11-Subunit Bovine Mitochondrial Cytochrome bc1 Complex journal, July 1998

Protein conformational changes involved in the cytochrome bc1 complex catalytic cycle journal, November 2013

The quinone chemistry of bc complexes journal, July 2004

The complex architecture of oxygenic photosynthesis journal, December 2004

Direct Demonstration of Half-of-the-sites Reactivity in the Dimeric Cytochrome bc1 Complex journal, January 2010

Antimycin-type depsipeptides: discovery, biosynthesis, chemical synthesis, and bioactivities journal, January 2016

Evolution of cytochrome bc complexes: From membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates journal, November 2013

Structure-Function of the Cytochrome b 6 f Complex † journal, November 2008

Differential activities of heterocyst ferredoxin, vegetative cell ferredoxin, and flavodoxin as electron carriers in nitrogen fixation and photosynthesis in Anabaena sp. journal, January 1995

Effects of Inhibitors on the Activity of the Cytochrome b6f Complex: Evidence for the Existence of Two Binding Pockets in the Lumenal Site journal, September 1999

Oxidation-reduction potentials of ferredoxin-NADP+ reductase and flavodoxin from Anabaena PCC 7119 and their electrostatic and covalent complexes journal, December 1991

The Mode of Action of UK-2A and UK-3A, Novel Antifungal Antibiotics from Streptomyces sp. 517-02. journal, January 1997

Properties of a semiquinone anion located in the QH 2 :Cytochrome c oxidoreductase segment of the mitochondrial respiratory chain journal, December 1980

The transient complex of poplar plastocyanin with cytochrome f: effects of ionic strength and pH journal, April 2005

Ubiquinone in Rhodopseudomonas sphaeroides. Some thermodynamic properties journal, April 1979

The protein moiety modulates the redox potential in cytochromes c journal, January 1994

Signal Transduction between the Chloroplast and the Nucleus journal, May 2002

Membrane potential-linked reversed electron transfer in the beef heart cytochrome bc1 complex reconstituted into potassium-loaded phospholipid vesicles. journal, January 1994

Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins journal, December 2003

A motif for quinone binding sites in respiratory and photosynthetic systems 1 1Edited by R. Huber journal, March 2000

Title: Catalytic Reactions and Energy Conservation in the Cytochrome bc₁ and b₆f Complexes of Energy-Transducing Membranes

Kinetics of oxidation of hydroquinones by molecular oxygen. Effect of superoxide dismutase
journal, January 2000

Molecular Organization of Cytochrome c ₂ near the Binding Domain of Cytochrome bc ₁ Studied by Electron Spin–Lattice Relaxation Enhancement
journal, June 2014

Famoxadone: the discovery and optimisation of a new agricultural fungicide
journal, January 2001

Stigmatellin, a new antibiotic from Stigmatella aurantiaca (Myxobacterales). I. Production, physico-chemical and biological properties.
journal, January 1984

First Evidence for Existence of an Uphill Electron Transfer through the bc1 and NADH-Q Oxidoreductase Complexes of the Acidophilic Obligate Chemolithotrophic Ferrous Ion-Oxidizing Bacterium Thiobacillus ferrooxidans
journal, June 2000

Use of a Photoactivated Ruthenium Dimer Complex To Measure Electron Transfer between the Rieske Iron−Sulfur Protein and Cytochrome c ₁ in the Cytochrome bc ₁ Complex ^†
journal, April 2000

The cellular production of hydrogen peroxide
journal, July 1972

Intermonomer Electron Transfer between the Low-Potential b Hemes of Cytochrome bc ₁
journal, March 2011

Monitoring cytochrome redox changes in the mitochondria of intact cells using multi-wavelength visible light spectroscopy
journal, December 2003

The heme redox center of chloroplast cytochrome f is linked to a buried five-water chain
journal, June 1996

Photosynthetic growth despite a broken Q-cycle
journal, May 2011

Orientation of the g - Tensor Axes of the Rieske Subunit in the Cytochrome bc ₁ Complex ^†
journal, January 2004

Why is it so difficult to construct Qi site mutants in Chlamydomonas reinhardtii?
journal, July 2008

Drought stress-induced upregulation of components involved in ferredoxin-dependent cyclic electron transfer
journal, August 2010

Electrochemical and Spectroscopic Investigations of the Cytochrome bc ₁ Complex from Rhodobacter capsulatus ^†
journal, October 1999

Effects of dibromothymoquinone on the structure and function of the mitochondrial bc1 complex
journal, October 1984

The Isolation and Properties of Antimycin A
journal, July 1949

Ascochlorin, a new Antibiotic, Found by Paper-Disc Agar-Diffusion Method. i
journal, January 1968

Reactions of the semiquinone free radicals of anti-tumour agents with oxygen and iron complexes
journal, March 1985

Proton pump coupled to cytochrome c oxidase in mitochondria
journal, March 1977

PGR5-PGRL1-Dependent Cyclic Electron Transport Modulates Linear Electron Transport Rate in Arabidopsis thaliana
journal, February 2016

A semiquinone intermediate generated at the Qo site of the cytochrome bc1 complex: Importance for the Q-cycle and superoxide production
journal, April 2007

A new concept for ferredoxin–NADP(H) oxidoreductase binding to plant thylakoids
journal, November 2010

Transient inactivation of the thylakoid photosystem II light-harvesting protein kinase system and concomitant changes in intramembrane particle size during photoinhibition of Chlamydomonas reinhardtii.
journal, July 1986

Stigmatellin. A dual type inhibitor of photosynthetic electron transport
journal, May 1985

Interaction of positively charged amino acid residues of recombinant, cyanobacterial ferredoxin:NADP+ reductase with ferredoxin probed by site directed mutagenesis
journal, January 1998

Modification of inhibitor binding sites in the cytochrome bf complex by directed mutagenesis of cytochrome b6 in Synechococcus sp. PCC 7002
journal, April 2001

Redox properties of the DBMIB-Rieske iron-sulfur complex in spinach chloroplast membranes
journal, August 1981

Study of Inhibitory Effects and Action Mechanism of the Novel Fungicide Pyrimorph against Phytophthora capsici ^†
journal, March 2010

The End of the Line: Can Ferredoxin and Ferredoxin NADP(H) Oxidoreductase Determine the Fate of Photosynthetic Electrons?
journal, April 2014

An evolutionary analysis of the reaction mechanisms of photosystem I reduction by cytochrome c6 and plastocyanin
journal, January 2002

The cyclic electron pathways around photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage
journal, March 1994

Discovery of cytochrome bc ₁ complex inhibitors inspired by the natural product karrikinolide
journal, January 2016

Probing the Role of E272 in Quinol Oxidation of Mitochondrial Complex III ^†
journal, August 2006

Loss of Phylloquinone in Chlamydomonas Affects Plastoquinone Pool Size and Photosystem II Synthesis
journal, March 2007

The involvement of ferredoxin-NADP+ reductase in cyclic electron transport in chloroplasts
journal, July 1981

Structural aspects of the cytochromeb 6 f complex; structure of the lumen-side domain of cytochromef
journal, February 1994

Purification of highly active cytochrome bc1 complexes from phylogenetically diverse species by a single chromatographic procedure
journal, May 1987

On the Mechanism of Quinol Oxidation in thebc1 Complex
journal, August 1998

Protein−Protein Interactions between Cytochrome b and the Fe-S Protein Subunits during QH ₂ Oxidation and Large-Scale Domain Movement in the bc ₁ Complex ^†
journal, February 2003

Intraprotein transfer of the quinone analogue inhibitor 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone in the cytochrome b6f complex
journal, December 2005

The Q-cycle reviewed: How well does a monomeric mechanism of the bc1 complex account for the function of a dimeric complex?
journal, July 2008

Association of Ferredoxin:NADP+ oxidoreductase with the photosynthetic apparatus modulates electron transfer in Chlamydomonas reinhardtii
journal, June 2017

On the Redox Potentials of Ubiquinone and Cytochrome b in the Respiratory Chain
journal, July 1969

Design of anti-parasitic and anti-fungal hydroxy-naphthoquinones that are less susceptible to drug resistance
journal, May 2011

AS2077715 is a selective inhibitor of fungal mitochondrial cytochrome bc1 complex
journal, May 2014

The Modified Q-cycle Explains the Apparent Mismatch between the Kinetics of Reduction of Cytochromes c ₁ and b _H in the bc ₁ Complex
journal, June 2003

Antimalarial 4(1H)-pyridones bind to the Q _i site of cytochrome bc ₁
journal, January 2015

Membrane-Anchored Cytochrome c _y Mediated Microsecond Time Range Electron Transfer from the Cytochrome bc ₁ Complex to the Reaction Center in Rhodobacter c apsulatus ^†
journal, April 1998

UK-2A, B, C and D, Novel Antifungal Antibiotics from Streptomyces sp. 517-02. V. Inhibition Mechanism of Bovine Heart Mitochondrial Cytochrome bc1 by the Novel Antibiotic UK-2A.
journal, January 1999

Role of Chloroplast Protein Kinase Stt7 in LHCII Phosphorylation and State Transition in Chlamydomonas
journal, March 2003

Divergent pathways of photosynthetic electron transfer: The autonomous oxygenic and anoxygenic photosystems
journal, November 1995

Molecular Quantum Dot Cellular Automata Based on Diboryl Monoradical Anions
journal, January 2018

Myxothiazol, a new inhibitor of the cytochrome b-c1 segment of the respiratory chain
journal, December 1981

Distance metrics for heme protein electron tunneling
journal, July 2008

The reaction domain on Rhodospirillum rubrum cytochrome c2 and horse cytochrome c for the Rhodospirillum rubrum cytochrome bc1 complex.
journal, October 1987

Single catalytic site model for the oxidation of ferrocytochrome c by mitochondrial cytochrome c oxidase.
journal, January 1984

Complete Structure of the 11-Subunit Bovine Mitochondrial Cytochrome bc1 Complex
journal, July 1998

Protein conformational changes involved in the cytochrome bc1 complex catalytic cycle
journal, November 2013

The quinone chemistry of bc complexes
journal, July 2004

The complex architecture of oxygenic photosynthesis
journal, December 2004

Direct Demonstration of Half-of-the-sites Reactivity in the Dimeric Cytochrome bc1 Complex
journal, January 2010

Antimycin-type depsipeptides: discovery, biosynthesis, chemical synthesis, and bioactivities
journal, January 2016

Evolution of cytochrome bc complexes: From membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates
journal, November 2013

Structure-Function of the Cytochrome b ₆ f Complex ^†
journal, November 2008

Differential activities of heterocyst ferredoxin, vegetative cell ferredoxin, and flavodoxin as electron carriers in nitrogen fixation and photosynthesis in Anabaena sp.
journal, January 1995

Effects of Inhibitors on the Activity of the Cytochrome b₆f Complex: Evidence for the Existence of Two Binding Pockets in the Lumenal Site
journal, September 1999

Oxidation-reduction potentials of ferredoxin-NADP+ reductase and flavodoxin from Anabaena PCC 7119 and their electrostatic and covalent complexes
journal, December 1991

The Mode of Action of UK-2A and UK-3A, Novel Antifungal Antibiotics from Streptomyces sp. 517-02.
journal, January 1997

Properties of a semiquinone anion located in the QH ₂ :Cytochrome c oxidoreductase segment of the mitochondrial respiratory chain
journal, December 1980

The transient complex of poplar plastocyanin with cytochrome f: effects of ionic strength and pH
journal, April 2005

Ubiquinone in Rhodopseudomonas sphaeroides. Some thermodynamic properties
journal, April 1979

The protein moiety modulates the redox potential in cytochromes c
journal, January 1994

Signal Transduction between the Chloroplast and the Nucleus
journal, May 2002

Membrane potential-linked reversed electron transfer in the beef heart cytochrome bc1 complex reconstituted into potassium-loaded phospholipid vesicles.
journal, January 1994

Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins
journal, December 2003

A motif for quinone binding sites in respiratory and photosynthetic systems 1 1Edited by R. Huber
journal, March 2000

Solution structure of cytochrome c6 from the thermophilic cyanobacterium Synechococcus elongatus
journal, January 1998

Identification of the BAL-labile factor
journal, December 1980