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Structure–function of the cytochrome b6f lipoprotein complex: a scientific odyssey and personal perspective

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Abstract

Structure–function studies of the cytochrome b6f complex, the central hetero-oligomeric membrane protein complex in the electron transport chain of oxygenic photosynthesis, which formed the basis for a high-resolution (2.5 Å) crystallographic solution of the complex, are described. Structure–function differences between the structure of subunits of the bc complexes, b6f, and bc1 from mitochondria and photosynthetic bacteria, which are often assumed to function identically, are discussed. Major differences which suggest that quinone-dependent electron transport pathways can vary in b6f and bc1 complexes are as follows: (a) an additional c-type heme, cn, and bound single copies of chlorophyll a and β-carotene in the b6f complex; and (b) a cyclic electron transport pathway that encompasses the b6f and PSI reaction center complexes. The importance of including lipid in crystallization of the cytochrome complex, or with any hetero-oligomeric membrane protein complex, is emphasized, and consequences to structure–function of b6f being a lipoprotein complex discussed, including intra-protein dielectric heterogeneity and resultant pathways of trans-membrane electron transport. The role of the b6f complex in trans-membrane signal transduction from reductant generated on the p-side of the electron transport chain to the regulation of light energy to the two photosystems by trans-side phosphorylation of the light-harvesting chlorophyll protein is presented. Regarding structure aspects relevant to plastoquinol-quinone entrance-egress: (i) modification of the p-side channel for plastoquinone access to the iron-sulfur protein would change the rate-limiting step in electron transport; (ii) the narrow niche for entry of plastoquinol into b6f from the PSII reaction center complex would seem to require close proximity between the complexes.

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Abbreviations

CD:

Circular dichroism

Chl:

Chlorophyll

Cyt:

Cytochrome

n, p:

Electrochemically negative, positive sides of membrane

DOPC:

Dioleoyl-phosphatidyl choline

EPR:

Electron paramagnetic resonance

ISP:

Iron-sulfur protein

PDB:

Protein data base

PET:

Photosynthetic electron transfer

PQ, PQH2 :

Plastoquinone, -ol

PSI, PSII:

Photosystems I, II

TMH:

Trans-membrane helix

UDM:

n-undecyl-β-d-malto-pyranoside

\(\Delta {\tilde \mu }_{{\text{H}}^+}\) :

Trans-membrane proton electrochemical potential gradient

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Acknowledgements

Colleagues, whose studies have contributed to the information and concepts obtained in our laboratory in recent years, are reported here: R. Agarwal7, D. Baniulis6, S. Bhaduri1, S. Saif Hasan1, D. Huang (deceased), G. Kurisu9, S. Naurin1, S. Savikhin2, S. K. Singh8, J. L. Smith11, V. Stadnytskyi2,3, A. Szczepaniak12, J.P. Whitelegge5, E. Yamashita10, S.D. Zakharov1, M. Zhalnina and H. Zhang4 who are presently associated, respectively, with the Departments of Biological Sciences1 and Physics2 Purdue University; 3Lab of Chemical Physics, NIDDK, National Institutes of Health, Bethesda, MD USA; 4SSCI, West Lafayette, IN; 5Pasarow Mass Spectrometry Laboratory, NPI-Semel Institute, David Geffen School of Medicine, UCLA; 6Institute of Horticulture, Lithuanian Research Centre for Agriculture and Forestry, Lithuania; 7Molecular Biology Division, Bhabha Atomic Research Centre, Mumbai, India; 8Department of Biological Chemistry & Molecular Pharmacology, Harvard Medical School, Boston, MA; 9Lab. of Protein Crystallography, Lab. of Protein Databases (PDB), Institute for Protein Research, Osaka University; 10Institute for Protein Research, Osaka University, Japan;11Life Sciences Institute, University of Michigan; 12Dept. of Biotechnology, University of Wroclaw, Poland. Colleagues whose earlier studies provided the foundation for the information on structure–function of the cytochrome b6f complex described in third report: M. T. Black, H. Böhme, R. M. Everly, P. N. Furbacher, M. E. Girvin, P. Horton, L. I. Krishtalik, M. Ponomarev, G. S. Tae, J. Whitmarsh, and W. R. Widger. I thank Ms. G. Sincich for contributions to the illustrations, and express my gratitude to the NIH General Medical Sciences-038323, the Dept. of Energy, DOE (DE-SC0018238), and the Henry Koffler professorship, which have funded most of the research described here, and to the John Simon Guggenheim and Alexander von Humboldt Foundations for Fellowship support.

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    William A. Cramer

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Cramer, W.A. Structure–function of the cytochrome b6f lipoprotein complex: a scientific odyssey and personal perspective. Photosynth Res 139, 53–65 (2019). https://doi.org/10.1007/s11120-018-0585-x

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