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Internal lipid architecture of the hetero-oligomeric cytochrome b6f complex.

Hasan SS, Cramer WA
Structure 22 1008-15 (2014)
Cited: 23 times
EuropePMC logo PMID: 24931468

Abstract

The role of lipids in the assembly, structure, and function of hetero-oligomeric membrane protein complexes is poorly understood. The dimeric photosynthetic cytochrome b6f complex, a 16-mer of eight distinct subunits and 26 transmembrane helices, catalyzes transmembrane proton-coupled electron transfer for energy storage. Using a 2.5 Å crystal structure of the dimeric complex, we identified 23 distinct lipid-binding sites per monomer. Annular lipids are proposed to provide a connection for super-complex formation with the photosystem-I reaction center and the LHCII kinase enzyme for transmembrane signaling. Internal lipids mediate crosslinking to stabilize the domain-swapped iron-sulfur protein subunit, dielectric heterogeneity within intermonomer and intramonomer electron transfer pathways, and dimer stabilization through lipid-mediated intermonomer interactions. This study provides a complete structure analysis of lipid-mediated functions in a multi-subunit membrane protein complex and reveals lipid sites at positions essential for assembly and function.

Reviews - 4ogq mentioned but not cited (1)

  1. Structure-function of the cytochrome b6f lipoprotein complex: a scientific odyssey and personal perspective. Cramer WA. Photosynth Res 139 53-65 (2019)

Articles - 4ogq mentioned but not cited (10)

  1. Internal lipid architecture of the hetero-oligomeric cytochrome b6f complex. Hasan SS, Cramer WA. Structure 22 1008-1015 (2014)
  2. Probing the local lipid environment of the Rhodobacter sphaeroides cytochrome bc1 and Synechocystis sp. PCC 6803 cytochrome b6f complexes with styrene maleic acid. Swainsbury DJK, Proctor MS, Hitchcock A, Cartron ML, Qian P, Martin EC, Jackson PJ, Madsen J, Armes SP, Hunter CN. Biochim Biophys Acta Bioenerg 1859 215-225 (2018)
  3. Traffic within the cytochrome b6f lipoprotein complex: gating of the quinone portal. Hasan SS, Proctor EA, Yamashita E, Dokholyan NV, Cramer WA. Biophys J 107 1620-1628 (2014)
  4. Trans-membrane Signaling in Photosynthetic State Transitions: REDOX- AND STRUCTURE-DEPENDENT INTERACTION IN VITRO BETWEEN STT7 KINASE AND THE CYTOCHROME b6f COMPLEX. Singh SK, Hasan SS, Zakharov SD, Naurin S, Cohn W, Ma J, Whitelegge JP, Cramer WA. J Biol Chem 291 21740-21750 (2016)
  5. Emergence of cytochrome bc complexes in the context of photosynthesis. Dibrova DV, Shalaeva DN, Galperin MY, Mulkidjanian AY. Physiol Plant 161 150-170 (2017)
  6. Role of domain swapping in the hetero-oligomeric cytochrome b6f lipoprotein complex. Agarwal R, Hasan SS, Jones LM, Stofleth JT, Ryan CM, Whitelegge JP, Kehoe DM, Cramer WA. Biochemistry 54 3151-3163 (2015)
  7. Cryo-EM structures of the Synechocystis sp. PCC 6803 cytochrome b6f complex with and without the regulatory PetP subunit. Proctor MS, Malone LA, Farmer DA, Swainsbury DJK, Hawkings FR, Pastorelli F, Emrich-Mills TZ, Siebert CA, Hunter CN, Johnson MP, Hitchcock A. Biochem J 479 1487-1503 (2022)
  8. Catalytic Reactions and Energy Conservation in the Cytochrome bc1 and b6f Complexes of Energy-Transducing Membranes. Sarewicz M, Pintscher S, Pietras R, Borek A, Bujnowicz Ł, Hanke G, Cramer WA, Finazzi G, Osyczka A. Chem Rev 121 2020-2108 (2021)
  9. Isothermal titration calorimetry of membrane protein interactions: FNR and the cytochrome b6f complex. Zakharov SD, Savikhin S, Misumi Y, Kurisu G, Cramer WA. Biophys J 121 300-308 (2022)
  10. Structural and functional contributions of lipids to the stability and activity of the photosynthetic cytochrome b 6 f lipoprotein complex. Bhaduri S, Zhang H, Erramilli S, Cramer WA. J Biol Chem 294 17758-17767 (2019)


Articles citing this publication (12)

  1. Activation of the Stt7/STN7 Kinase through Dynamic Interactions with the Cytochrome b6f Complex. Shapiguzov A, Chai X, Fucile G, Longoni P, Zhang L, Rochaix JD. Plant Physiol 171 82-92 (2016)
  2. Cryo-EM structure of the spinach cytochrome b6 f complex at 3.6 Å resolution. Malone LA, Qian P, Mayneord GE, Hitchcock A, Farmer DA, Thompson RF, Swainsbury DJK, Ranson NA, Hunter CN, Johnson MP. Nature 575 535-539 (2019)
  3. A map of dielectric heterogeneity in a membrane protein: the hetero-oligomeric cytochrome b6f complex. Hasan SS, Zakharov SD, Chauvet A, Stadnytskyi V, Savikhin S, Cramer WA. J Phys Chem B 118 6614-6625 (2014)
  4. A stromal region of cytochrome b6f subunit IV is involved in the activation of the Stt7 kinase in Chlamydomonas. Dumas L, Zito F, Blangy S, Auroy P, Johnson X, Peltier G, Alric J. Proc Natl Acad Sci U S A 114 12063-12068 (2017)
  5. Natively oxidized amino acid residues in the spinach cytochrome b 6 f complex. Taylor RM, Sallans L, Frankel LK, Bricker TM. Photosynth Res 137 141-151 (2018)
  6. Chlorophyll a is the crucial redox sensor and transmembrane signal transmitter in the cytochrome b6f complex. Components and mechanisms of state transitions from the hydrophobic mismatch viewpoint. Vladkova R. J Biomol Struct Dyn 34 824-854 (2016)
  7. GreenCut protein CPLD49 of Chlamydomonas reinhardtii associates with thylakoid membranes and is required for cytochrome b6 f complex accumulation. Wittkopp TM, Saroussi S, Yang W, Johnson X, Kim RG, Heinnickel ML, Russell JJ, Phuthong W, Dent RM, Broeckling CD, Peers G, Lohr M, Wollman FA, Niyogi KK, Grossman AR. Plant J 94 1023-1037 (2018)
  8. Structural roles of lipid molecules in the assembly of plant PSII-LHCII supercomplex. Sheng X, Liu X, Cao P, Li M, Liu Z. Biophys Rep 4 189-203 (2018)
  9. Thylakoid membrane lipid sulfoquinovosyl-diacylglycerol (SQDG) is required for full functioning of photosystem II in Thermosynechococcus elongatus. Nakajima Y, Umena Y, Nagao R, Endo K, Kobayashi K, Akita F, Suga M, Wada H, Noguchi T, Shen JR. J Biol Chem 293 14786-14797 (2018)
  10. A novel chloroplast super-complex consisting of the ATP synthase and photosystem I reaction center. Bhaduri S, Singh SK, Cohn W, Hasan SS, Whitelegge JP, Cramer WA. PLoS One 15 e0237569 (2020)
  11. Efficient screening of protein-ligand complexes in lipid bilayers using LoCoMock score. Morita R, Shigeta Y, Harada R. J Comput Aided Mol Des 37 217-225 (2023)
  12. Non-detergent isolation of a cyanobacterial photosystem I using styrene maleic acid alternating copolymers. Brady NG, Li M, Ma Y, Gumbart JC, Bruce BD. RSC Adv 9 31781-31796 (2019)


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