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An Atypical Haem In The Cytochrome B6f Complex

David Stroebel, Y. Choquet, J. Popot, D. Picot
Published 2003 · Biology, Medicine

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Photosystems I and II (PSI and II) are reaction centres that capture light energy in order to drive oxygenic photosynthesis; however, they can only do so by interacting with the multisubunit cytochrome b6f complex. This complex receives electrons from PSII and passes them to PSI, pumping protons across the membrane and powering the Q-cycle. Unlike the mitochondrial and bacterial homologue cytochrome bc1, cytochrome b6f can switch to a cyclic mode of electron transfer around PSI using an unknown pathway. Here we present the X-ray structure at 3.1 Å of cytochrome b6f from the alga Chlamydomonas reinhardtii. The structure bears similarities to cytochrome bc1 but also exhibits some unique features, such as binding chlorophyll, β-carotene and an unexpected haem sharing a quinone site. This haem is atypical as it is covalently bound by one thioether linkage and has no axial amino acid ligand. This haem may be the missing link in oxygenic photosynthesis.
This paper references
10.1126/SCIENCE.1081397
Role of Chloroplast Protein Kinase Stt7 in LHCII Phosphorylation and State Transition in Chlamydomonas
Nathalie Depège (2003)
Liebigs Annal. Chem
(1984)
10.1093/emboj/20.23.6591
Specific roles of protein–phospholipid interactions in the yeast cytochrome bc1 complex structure
C. Lange (2001)
10.1074/jbc.272.35.21901
On the Presence and Role of a Molecule of Chlorophylla in the Cytochromeb 6  f Complex*
Y. Pierre (1997)
10.1074/jbc.272.51.32427
Molecular Genetic Identification of a Pathway for Heme Binding to Cytochrome b 6 *
R. Kuras (1997)
10.1111/J.1432-1033.1981.TB06379.X
A cytochrome f/b6 complex of five polypeptides with plastoquinol-plastocyanin-oxidoreductase activity from spinach chloroplasts.
E. Hurt (1981)
J. Theor. Biol
(1976)
10.1016/0003-2697(87)90643-9
Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra.
E. Berry (1987)
10.1006/JMBI.2000.3915
Early evolution of cytochrome bc complexes.
M. Schuetz (2000)
10.1107/S0108767390010224
Improved methods for building protein models in electron density maps and the location of errors in these models.
T. Jones (1991)
10.1021/BI980238O
Glu78, from the conserved PEWY sequence of subunit IV, has a key function in cytochrome b6f turnover.
F. Zito (1998)
10.1016/0005-2728(87)90235-0
On the nature of the g = 6 EPR signal in isolated cytochrome b6f complex from spinach chloroplasts
W. Nitschke (1987)
Supplementary Information accompanies the paper on www.nature.com/nature
10.1021/BI0004596
Interruption of the internal water chain of cytochrome f impairs photosynthetic function.
G. Sainz (2000)
10.1016/0304-4173(83)90004-6
The electrochemical domain of photosynthesis
A. Crofts (1983)
Structure at 2.3 Å resolution of the cytochrome bc1 complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody
C. Hunte (2000)
10.1021/BI980546M
In vivo analysis of the effect of dicyclohexylcarbodiimide on electron and proton transfers in cytochrome bf complex of Chlorella sorokiniana.
P. Joliot (1998)
10.1016/S0968-0004(01)01897-7
Large scale domain movement in cytochrome bc(1): a new device for electron transfer in proteins.
E. Darrouzet (2001)
10.1021/BI025714W
Redox-coupled proton pumping activity in cytochrome b6f, as evidenced by the pH dependence of electron transfer in whole cells of Chlamydomonas reinhardtii.
G. Finazzi (2002)
10.1074/JBC.M105454200
Ferredoxin:NADP+ oxidoreductase is a subunit of the chloroplast cytochrome b6f complex.
Hui Bin Zhang (2001)
Jean-Luc.Popot@ibpc.fr) Coordinates and structure factors have been deposited with the PDB under accession code 1Q90
J.-L P
10.1074/JBC.270.49.29342
Purification and Characterization of the Cytochrome b6 f Complex from Chlamydomonas reinhardtii*
Y. Pierre (1995)
The cytochrome b(6)f complex: structural studies and comparison with the bc(1) complex.
C. Breyton (2000)
10.1016/S0005-2728(00)00185-7
The cytochrome b6f complex: structural studies and comparison with the bc1 complex
C. Breyton (2000)
10.1021/BI020674H
Role of charges on cytochrome f from the cyanobacterium Phormidium laminosum in its interaction with plastocyanin.
S. E. Hart (2003)
10.1111/J.1432-1033.1989.TB14494.X
An atypical heme-binding structure of cytochrome c1 of Euglena gracilis mitochondrial complex III.
K. Mukai (1989)
10.1073/PNAS.95.3.1319
The plastid ndh genes code for an NADH-specific dehydrogenase: isolation of a complex I analogue from pea thylakoid membranes.
L. Sazanov (1998)
10.1016/0022-5193(76)90124-7
Possible molecular mechanisms of the protonmotive function of cytochrome systems.
P. Mitchell (1976)
10.1073/PNAS.96.18.10021
Pathways for proton release during ubihydroquinone oxidation by the bc(1) complex.
A. Crofts (1999)
10.1002/JLAC.198419841202
Antibiotika aus Gleitenden Bakterien, XXIII. Stigmatellin A und B — zwei neue Antibiotika aus Stigmatella aurantiaca (Myxobacterales)
G. Hoefle (1984)
10.1126/SCIENCE.277.5322.60
Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria.
D. Xia (1997)
10.1074/JBC.275.8.5275
On the Spatial Organization of Hemes and Chlorophyll in Cytochrome b 6 f
B. Schoepp (2000)
10.1016/S0969-2126(00)00152-0
Structure at 2.3 A resolution of the cytochrome bc(1) complex from the yeast Saccharomyces cerevisiae co-crystallized with an antibody Fv fragment.
C. Hunte (2000)
Correspondence and requests for materials should be addressed to M.L.L. (email:
10.1074/jbc.272.35.21892
Dimer to Monomer Conversion of the Cytochromeb 6  f Complex
C. Breyton (1997)
10.1016/0005-2728(93)90210-7
The chloroplast cytochrome bf complex: a critical focus on function.
A. Hope (1993)
10.1105/tpc.011692
Cytochrome f Translation in Chlamydomonas Chloroplast Is Autoregulated by its Carboxyl-Terminal Domain Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011692.
Y. Choquet (2003)
Programs for protein crystallography
The CCP4 suite (1994)
10.1021/BI9825448
Assignment of the heme axial ligand(s) for the ferric myoglobin (H93G) and heme oxygenase (H25A) cavity mutants as oxygen donors using magnetic circular dichroism.
A. Pond (1999)
10.1016/S0005-2728(01)00212-2
The presence of 9-cis-β-carotene in cytochrome b6f complex from spinach
J. Yan (2001)
10.1016/0005-2728(88)90039-4
The low-potential electron-transfer chain in the cytochrome bf complex
P. Joliot (1988)
10.1126/SCIENCE.281.5373.64
Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex.
S. Iwata (1998)
cytochrome b 6f complex from spinach and the cyanobacterium Mastigocladus laminosus
J. P. Whitelegge (2002)
10.1093/emboj/20.14.3623
State transitions reveal the dynamics and flexibility of the photosynthetic apparatus
F. Wollman (2001)
10.1038/33612
Electron transfer by domain movement in cytochrome bc1
Z. Zhang (1998)
10.1074/JBC.273.15.8860
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. Yu (1998)
Causes and Consequences
Michael Marcus (1969)
10.1107/S0907444998003254
Crystallography & NMR system: A new software suite for macromolecular structure determination.
A. Brünger (1998)
10.1016/S0969-2126(97)00309-2
Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein.
C. Carrell (1997)
10.1016/S0076-6879(97)77028-9
Raster3D: photorealistic molecular graphics.
E. Merritt (1997)
a critical focus on function
Hope (1993)
10.1107/S0021889891004399
A program to produce both detailed and schematic plots of protein structures
P. Kraulis (1991)
Competing interests statement The authors declare that they have no competing financial interests
10.1016/S0006-3495(98)77523-X
Fluorescence and absorption spectroscopy of the weakly fluorescent chlorophyll a in cytochrome b6f of Synechocystis PCC6803.
E. Peterman (1998)
10.1074/mcp.M200045-MCP200
Full Subunit Coverage Liquid Chromatography Electrospray Ionization Mass Spectrometry (LCMS+) of an Oligomeric Membrane Protein
J. Whitelegge (2002)
10.1016/0005-2728(83)90220-7
Membrane potential-dependent reduction of cytochrome b-6 in an algal mutant lacking Photosystem I centers
J. Lavergne (1983)
10.1016/S0969-2126(00)00012-5
Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation.
S. Martinez (1994)
Tuning the cavity
G. Kurisu
10.1074/jbc.274.3.1581
Stoichiometrically Bound β-Carotene in the Cytochromeb6f Complex of Oxygenic Photosynthesis Protects against Oxygen Damage*
Hui Bin Zhang (1999)
10.1126/SCIENCE.1090165
Structure of the Cytochrome b6f Complex of Oxygenic Photosynthesis: Tuning the Cavity
G. Kurisu (2003)
10.1073/pnas.0931431100
A defined protein–detergent–lipid complex for crystallization of integral membrane proteins: The cytochrome b6f complex of oxygenic photosynthesis
H. Zhang (2003)
10.1021/BI002090Q
Replacement of the axial histidine ligand with imidazole in cytochrome c peroxidase. 2. Effects on heme coordination and function.
J. Hirst (2001)
The CCP 4 Suite — Computer programs for protein crystallography
L. Lally (1998)
10.1083/JCB.47.2.332
PROTONATION AND CHLOROPLAST MEMBRANE STRUCTURE
Satoru Murakami (1970)
10.1074/JBC.272.35.21892
Dimer to monomer conversion of the cytochrome b6 f complex. Causes and consequences.
C. Breyton (1997)



This paper is referenced by
10.1080/13102818.2008.10817522
Characterization and Stabilization of Solubilized Membrane Proteins
C. Ebel (2008)
10.1016/J.CHEMPHYSLIP.2006.02.005
Lipid conformation in crystalline bilayers and in crystals of transmembrane proteins.
D. Marsh (2006)
10.1016/j.plaphy.2008.01.003
Crystal structure of cyanobacterial photosystem II at 3.0 A resolution: a closer look at the antenna system and the small membrane-intrinsic subunits.
F. Müh (2008)
10.1016/J.TIBS.2005.02.001
Fixing the Q cycle.
A. Osyczka (2005)
Deg- und SppA-Proteasen als Komponenten langfristiger physiologischer Anpassung des Photosynthesesapparates
Irina Sterr (2006)
10.1074/JBC.M503319200
The Iron-Sulfur Cluster of the Rieske Iron-Sulfur Protein Functions as a Proton-exiting Gate in the Cytochrome bc1 Complex*
B. Gurung (2005)
10.1016/j.tplants.2010.05.012
The cell biology of tetrapyrroles: a life and death struggle.
N. Mochizuki (2010)
10.1093/pcp/pcq085
De novo biosynthesis of fatty acids plays critical roles in the response of the photosynthetic machinery to low temperature in Arabidopsis.
T. Takami (2010)
10.1074/jbc.M809196200
Structure-Function, Stability, and Chemical Modification of the Cyanobacterial Cytochrome b6f Complex from Nostoc sp. PCC 7120*
D. Baniulis (2009)
10.1007/978-1-4020-8815-5_23
The Cytochrome bc 1 and Related bc Complexes: The Rieske/Cytochrome b Complex as the Functional Core of a Central Electron/Proton Transfer Complex
D. Kramer (2009)
10.1016/J.BBABIO.2005.11.010
Design and engineering of photosynthetic light-harvesting and electron transfer using length, time, and energy scales.
D. Noy (2006)
10.1016/j.crvi.2008.04.003
Why is it so difficult to construct Q(i) site mutants in Chlamydomonas reinhardtii?
Agnès de Lacroix de Lavalette (2008)
10.1016/j.jmb.2011.09.023
Conservation of lipid functions in cytochrome bc complexes.
S. Hasan (2011)
10.1016/j.bbabio.2016.03.028
Exploring membrane respiratory chains.
Bruno C. Marreiros (2016)
10.1074/mcp.M114.040923
Deciphering Thylakoid Sub-compartments using a Mass Spectrometry-based Approach*
Martino Tomizioli (2014)
10.1111/tpj.13999
In vivo lipid ‘tag and track’ approach shows acyl editing of plastid lipids and chloroplast import of phosphatidylglycerol precursors in Arabidopsis thaliana
Anna K. Hurlock (2018)
10.2210/PDB6RQF/PDB
Cryo-EM structure of the spinach cytochrome b6f complex at 3.6 angstrom resolution.
L. A. Malone (2019)
10.1016/j.jmb.2008.05.066
Quinol oxidation by c-type cytochromes: structural characterization of the menaquinol binding site of NrfHA.
M. L. Rodrigues (2008)
10.1021/acs.jpcb.6b11709
Pathways of Transmembrane Electron Transfer in Cytochrome bc Complexes: Dielectric Heterogeneity and Interheme Coulombic Interactions.
S. Bhaduri (2017)
10.1007/978-90-481-2863-1_7
Molecular Genetics of Lipid Metabolism in the Model Green Alga Chlamydomonas reinhardtii
Eric R. Moellering (2009)
10.1104/pp.110.166652
The Importance of Energy Balance in Improving Photosynthetic Productivity1[W]
D. Kramer (2010)
10.1021/bi301638h
Lipid-induced conformational changes within the cytochrome b6f complex of oxygenic photosynthesis.
S. Hasan (2013)
10.1073/pnas.1222248110
Quinone-dependent proton transfer pathways in the photosynthetic cytochrome b6f complex
S. Hasan (2013)
10.1074/jbc.M606436200
Knock-out of the Plastid-encoded PetL Subunit Results in Reduced Stability and Accelerated Leaf Age-dependent Loss of the Cytochrome b6f Complex*
M. A. Schöttler (2007)
10.1016/B978-0-12-378630-2.00158-4
[Structure and function of the cytochrome b6f complex of oxygenic photosynthesis].
G. Kurisu (2004)
10.1016/J.TRAC.2005.04.010
Tandem mass spectrometry of integral membrane proteins for top-down proteomics
J. Whitelegge (2005)
10.1105/tpc.105.030676
The Light Reactions: A Guide to Recent Acquisitions for the Picture Gallery
S. Merchant (2005)
10.1093/pcp/pcq173
Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions.
C. Miyake (2010)
10.1021/BI036093P
Biochemical and spectroscopic characterization of the covalent binding of heme to cytochrome b6.
C. de Vitry (2004)
10.3390/md9061101
Carotenoids in Algae: Distributions, Biosyntheses and Functions
S. Takaichi (2011)
10.1007/978-3-642-53971-8_50
Algal Photosynthesis, Biosorption, Biotechnology, and Biofuels
Ozcan Konur (2015)
10.1016/j.jprot.2017.09.015
Integrated physiological and proteomic analysis reveals underlying response and defense mechanisms of Brachypodium distachyon seedling leaves under osmotic stress, cadmium and their combined stresses.
Zhi-Wei Cheng (2018)
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