Characterization of the Rate-Limiting Steps in the Dark-To-Light Transitions of Closed Photosystem II: Temperature Dependence and Invariance of Waiting Times during Multiple Light Reactions

. 2022 Dec 21 ; 24 (1) : . [epub] 20221221

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36613535

Grantová podpora
OTKA K-128679 and PD-138498 Hungarian Ministry of Innovation and Technology, National Research, Development and Innovation Fund
2018-1.2.1-NKP-2018-00009 Hungarian Ministry of Innovation and Technology, National Research, Development and Innovation Fund
GA ČR 19-13637S Czech Science Foundation
ELKH KÖ-36/2021 Eötvös Loránd Research Network
2022YFA0911900, 2022YFC1803400 National Key R&D Program of China
YSBR-004 CAS Project for Young Scientists in Basic Research
XDA26050402 Strategic Priority Research Program of the Chinese Academy of Sciences
31470339 National Natural Science Foundation of China

Rate-limiting steps in the dark-to-light transition of Photosystem II (PSII) were discovered by measuring the variable chlorophyll-a fluorescence transients elicited by single-turnover saturating flashes (STSFs). It was shown that in diuron-treated samples: (i) the first STSF, despite fully reducing the QA quinone acceptor molecule, generated only an F1(

Zobrazit více v PubMed

Magyar M., Sipka G., Kovacs L., Ughy B., Zhu Q.J., Han G.Y., Spunda V., Lambrev P.H., Shen J.R., Garab G. Rate-limiting steps in the dark-to-light transition of Photosystem II—Revealed by chlorophyll-a fluorescence induction. Sci. Rep. 2018;8:2755. doi: 10.1038/s41598-018-21195-2. PubMed DOI PMC

Sipka G., Magyar M., Mezzetti A., Akhtar P., Zhu Q., Xiao Y., Han G., Santabarbara S., Shen J.-R., Lambrev P.H., et al. Light-Adapted Charge-Separated State of Photosystem II: Structural and Functional Dynamics of the Closed Reaction Center. Plant Cell. 2021;33:1286–1302. doi: 10.1093/plcell/koab008. PubMed DOI PMC

Nelson N., Yocum C.F. Structure and function of photosystems I and II. Annu. Rev. Plant Biol. 2006;57:521–565. doi: 10.1146/annurev.arplant.57.032905.105350. PubMed DOI

Romero E., Novoderezhkin V.I., van Grondelle R. Quantum design of photosynthesis for bio-inspired solar-energy conversion. Nature. 2017;543:355–365. doi: 10.1038/nature22012. PubMed DOI

Blankenship R.E. Molecular Mechanisms of Photosynthesis. Wiley; New York, NY, USA: 2021.

Shen J.R. The Structure of Photosystem II and the Mechanism of Water Oxidation in Photosynthesis. Annu. Rev. Plant Biol. 2015;66:23–48. doi: 10.1146/annurev-arplant-050312-120129. PubMed DOI

Umena Y., Kawakami K., Shen J.R., Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 angstrom. Nature. 2011;473:55–60. doi: 10.1038/nature09913. PubMed DOI

Cardona T., Sedoud A., Cox N., Rutherford A.W. Charge separation in Photosystem II: A comparative and evolutionary overview. BBA-Bioenerg. 2012;1817:26–43. doi: 10.1016/j.bbabio.2011.07.012. PubMed DOI

Shlyk-Kerner O., Samish I., Kaftan D., Holland N., Sai P.S.M., Kless H., Scherz A. Protein flexibility acclimatizes photosynthetic energy conversion to the ambient temperature. Nature. 2006;442:827–830. doi: 10.1038/nature04947. PubMed DOI

Lubitz W., Chrysina M., Cox N. Water oxidation in photosystem II. Photosynth. Res. 2019;142:105–125. doi: 10.1007/s11120-019-00648-3. PubMed DOI PMC

Hasan S.S., Cramer W.A. On rate limitations of electron transfer in the photosynthetic cytochrome b6f complex. Phys. Chem. Chem. Phys. 2012;14:13853–13860. doi: 10.1039/c2cp41386h. PubMed DOI PMC

Holland S.C., Kappell A.D., Burnap R.L. Redox changes accompanying inorganic carbon limitation in Synechocystis sp PCC 6803. BBA-Bioenerg. 2015;1847:355–363. doi: 10.1016/j.bbabio.2014.12.001. PubMed DOI

Zavrel T., Szabo M., Tamburic B., Evenhuis C., Kuzhiumparambil U., Literakova P., Larkum A.W.D., Raven J.A., Cerveny J., Ralph P.J. Effect of carbon limitation on photosynthetic electron transport in Nannochloropsis oculata. J. Photoch. Photobio. B. 2018;181:31–43. doi: 10.1016/j.jphotobiol.2018.02.020. PubMed DOI

Suga M., Akita F., Sugahara M., Kubo M., Nakajima Y., Nakane T., Yamashita K., Umena Y., Nakabayashi M., Yamane T., et al. Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature. 2017;543:131–135. doi: 10.1038/nature21400. PubMed DOI

Suga M., Akita F., Yamashita K., Nakajima Y., Ueno G., Li H., Yamane T., Hirata K., Umena Y., Yonekura S., et al. An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser. Science. 2019;366:334–338. doi: 10.1126/science.aax6998. PubMed DOI

Kern J., Chatterjee R., Young I.D., Fuller F.D., Lassalle L., Ibrahim M., Gul S., Fransson T., Brewster A.S., Alonso-Mori R., et al. Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature. 2018;563:421–425. doi: 10.1038/s41586-018-0681-2. PubMed DOI PMC

Stowell M.H., McPhillips T.M., Rees D.C., Soltis S.M., Abresch E., Feher G. Light-induced structural changes in photosynthetic reaction center: Implications for mechanism of electron-proton transfer. Science. 1997;276:812–816. doi: 10.1126/science.276.5313.812. PubMed DOI

Sugo Y., Saito K., Ishikita H. Mechanism of the formation of proton transfer pathways in photosynthetic reaction centers. Proc. Natl. Acad. Sci. USA. 2021;118:e2103203118. doi: 10.1073/pnas.2103203118. PubMed DOI PMC

Wei R.J., Zhang Y., Mao J., Kaur D., Khaniya U., Gunner M.R. Comparison of proton transfer paths to the Q(A) and Q(B) sites of the Rb. sphaeroides photosynthetic reaction centers. Photosynth. Res. 2022;152:153–165. doi: 10.1007/s11120-022-00906-x. PubMed DOI

Michel H., Deisenhofer J. Relevance of the Photosynthetic Reaction Center from Purple Bacteria to the Structure of Photosystem-II. Biochemistry. 1988;27:1–7. doi: 10.1021/bi00401a001. DOI

Heathcote P., Fyfe P.K., Jones M.R. Reaction centres: The structure and evolution of biological solar power. Trends Biochem. Sci. 2002;27:79–87. doi: 10.1016/S0968-0004(01)02034-5. PubMed DOI

Krammer E.M., Sebban P., Ullmann G.M. Profile Hidden Markov Models for Analyzing Similarities and Dissimilarities in the Bacterial Reaction Center and Photosystem II. Biochemistry. 2009;48:1230–1243. doi: 10.1021/bi802033k. PubMed DOI

Cardona T. Photosystem II is a Chimera of Reaction Centers. J. Mol. Evol. 2017;84:149–151. doi: 10.1007/s00239-017-9784-x. PubMed DOI

Van Mourik F., Frese R.N., van der Zwan G., Cogdell R.J., van Grondelle R. Direct observation of solvation dynamics and dielectric relaxation in the photosynthetic light-harvesting-2 complex of Rhodopseudomonas acidophila. J. Phys. Chem. B. 2003;107:2156–2161. doi: 10.1021/jp026726u. DOI

Deshmukh S.S., Tang K., Kalman L. Lipid binding to the carotenoid binding site in photosynthetic reaction centers. J. Am. Chem. Soc. 2011;133:16309–16316. doi: 10.1021/ja207750z. PubMed DOI

Deshmukh S.S., Williams J.C., Allen J.P., Kalman L. Light-induced conformational changes in photosynthetic reaction centers: Dielectric relaxation in the vicinity of the dimer. Biochemistry. 2011;50:340–348. doi: 10.1021/bi101496c. PubMed DOI

Kleinfeld D., Okamura M.Y., Feher G. Electron-Transfer Kinetics in Photosynthetic Reaction Centers Cooled to Cryogenic Temperatures in the Charge-Separated State—Evidence for Light-Induced Structural-Changes. Biochemistry. 1984;23:5780–5786. doi: 10.1021/bi00319a017. PubMed DOI

Abgaryan G.A., Christophorov L.N., Goushcha A.O., Holzwarth A.R., Kharkyanen V.N., Knox P.P., Lukashev E.A. Effects of mutual influence of photoinduced electron transitions and slow structural rearrangements in bacterial photosynthetic reaction centers. J. Biol. Phys. 1998;24:1–17. doi: 10.1023/A:1005039023702. PubMed DOI PMC

Goushcha A.O., Kharkyanen V.N., Scott G.W., Holzwarth A.R. Self-regulation phenomena in bacterial reaction centers. I. General theory. Biophys. J. 2000;79:1237–1252. doi: 10.1016/S0006-3495(00)76378-8. PubMed DOI PMC

Barabash Y.M., Berezetskaya N.M., Christophorov L.N., Goushcha A.O., Kharkyanen V.N. Effects of structural memory in protein reactions. J. Chem. Phys. 2002;116:4339–4352. doi: 10.1063/1.1447906. DOI

Christophorov L., Holzwarth A., Kharkyanen V. Conformational regulation in single molecule reactions. Ukr. J. Phys. 2003;48:672–680.

Goushcha A.O., Manzo A.J., Scott G.W., Christophorov L.N., Knox P.P., Barabash Y.M., Kapoustina M.T., Berezetska N.M., Kharkyanen V.N. Self-regulation phenomena applied to bacterial reaction centers 2. Nonequilibrium adiabatic potential: Dark and light conformations revisited. Biophys. J. 2003;84:1146–1160. doi: 10.1016/S0006-3495(03)74930-3. PubMed DOI PMC

Joliot P., Joliot A. Comparative-Study of the Fluorescence Yield and of the C550 Absorption Change at Room-Temperature. Biochim. Biophys. Acta. 1979;546:93–105. doi: 10.1016/0005-2728(79)90173-7. PubMed DOI

Laisk A., Oja V. Variable fluorescence of closed photochemical reaction centers. Photosynth. Res. 2020;143:335–346. doi: 10.1007/s11120-020-00712-3. PubMed DOI

Oja V., Laisk A. Time- and reduction-dependent rise of photosystem II fluorescence during microseconds-long inductions in leaves. Photosynth. Res. 2020;145:209–225. doi: 10.1007/s11120-020-00783-2. PubMed DOI

Sipka G., Muller P., Brettel K., Magyar M., Kovacs L., Zhu Q.J., Xiao Y.A., Han G.Y., Lambrev P.H., Shen J.R., et al. Redox transients of P680 associated with the incremental chlorophyll-a fluorescence yield rises elicited by a series of saturating flashes in diuron-treated photosystem II core complex of Thermosynechococcus vulcanus. Physiol. Plant. 2019;166:22–32. doi: 10.1111/ppl.12945. PubMed DOI

Andreasson U., Andreasson L.E. Characterization of a semi-stable, charge-separated state in reaction centers from Rhodobacter sphaeroides. Photosynth. Res. 2003;75:223–233. doi: 10.1023/A:1023944605460. PubMed DOI

Malferrari M., Mezzetti A., Francia F., Venturoli G. Effects of dehydration on light-induced conformational changes in bacterial photosynthetic reaction centers probed by optical and differential FTIR spectroscopy. BBA-Bioenerg. 2013;1827:328–339. doi: 10.1016/j.bbabio.2012.10.009. PubMed DOI

Strasser R.J., Srivastava A., Govindjee Polyphasic Chlorophyll-a Fluorescence Transient in Plants and Cyanobacteria. Photochem. Photobiol. 1995;61:32–42. doi: 10.1111/j.1751-1097.1995.tb09240.x. DOI

Govindjee G., Papageorgiou G. Chlorophyll A Fluorescence: A Signature of Photosynthesis. Springer; Dordrecht, The Netherlands: 2004. pp. 1–41.

Sipka G., Nagy L., Magyar M., Akhtar P., Shen J.-R., Holzwarth A.R., Lambrev P.H., Garab G. Light-induced reversible reorganizations in closed Type-II reaction centre complexes. Physiological roles and physical mechanisms. Open Biol. 2022;12:220297. doi: 10.1098/rsob.220297. PubMed DOI PMC

Magyar M., Akhtar P., Sipka G., Han W., Li X., Han G., Shen J.R., Lambrev P.H., Garab G. Dependence of the rate-limiting steps in the dark-to-light transition of photosystem II on the lipidic environment of the reaction center. Photosynthetica. 2022;60:147–156. doi: 10.32615/ps.2022.016. DOI

Jaenicke R., Bohm G. The stability of proteins in extreme environments. Curr. Opin. Struct. Biol. 1998;8:738–748. doi: 10.1016/S0959-440X(98)80094-8. PubMed DOI

Garbers A., Reifarth F., Kurreck J., Renger G., Parak F. Correlation between protein flexibility and electron transfer from QA to QB in PSII membrane fragments from spinach. Biochemistry. 1998;37:11399–11404. doi: 10.1021/bi980296+. PubMed DOI

Pieper J., Hauss T., Buchsteiner A., Baczynski K., Adamiak K., Lechner R.E., Renger G. Temperature- and hydration-dependent protein dynamics in photosystem II of green plants studied by quasielastic neutron scattering. Biochemistry. 2007;46:11398–11409. doi: 10.1021/bi700179s. PubMed DOI

Pieper J., Trapp M., Skomorokhov A., Natkaniec I., Peters J., Renger G. Temperature-dependent vibrational and conformational dynamics of photosystem II membrane fragments from spinach investigated by elastic and inelastic neutron scattering. BBA-Bioenerg. 2012;1817:1213–1219. doi: 10.1016/j.bbabio.2012.03.020. PubMed DOI

Nakanishi M., Sokolov A.P. Dielectric Spectroscopy of Hydrated Biomacromolecules. In: Raicu V., Feldman Y., editors. Dielectric Relaxation in Biological Systems: Physical Principles, Methods, and Applications. Oxford University Press; Oxford, UK: 2015. pp. 248–275.

Katona G., Snijder A., Gourdon P., Andreasson U., Hansson O., Andreasson L.E., Neutze R. Conformational regulation of charge recombination reactions in a photosynthetic bacterial reaction center. Nat. Struct. Mol. Biol. 2005;12:630–631. doi: 10.1038/nsmb948. PubMed DOI

Iwata T., Paddock M.L., Okamura M.Y., Kandori H. Identification of FTIR Bands Due to Internal Water Molecules around the Quinone Binding Sites in the Reaction Center from Rhodobacter sphaeroides. Biochemistry. 2009;48:1220–1229. doi: 10.1021/bi801990s. PubMed DOI PMC

Malferrari M., Turina P., Francia F., Mezzetti A., Leibl W., Venturoli G. Dehydration affects the electronic structure of the primary electron donor in bacterial photosynthetic reaction centers: Evidence from visible-NIR and light-induced difference FTIR spectroscopy. Photoch. Photobio. Sci. 2015;14:238–251. doi: 10.1039/c4pp00245h. PubMed DOI

Koike H., Inoue Y. Preparation of oxygen-evolving photosystem II particles from a thermophilic blue-green alga. In: Inoue Y., Crofts A.R., Govindjee M.N., Renger G., Satoh K., editors. The Oxygen Evolving System of Photosynthesis. Academic Press; Cambridge, MA, USA: 1983. pp. 257–263.

Shen J.R., Kawakami K., Koike H. Purification and crystallization of oxygen-evolving photosystem II core complex from thermophilic cyanobacteria. Methods Mol. Biol. 2011;684:41–51. doi: 10.1007/978-1-60761-925-3_5. PubMed DOI

Chylla R.A., Garab G., Whitmarsh J. Evidence for Slow Turnover in a Fraction of Photosystem-II Complexes in Thylakoid Membranes. Biochim. Biophys. Acta. 1987;894:562–571. doi: 10.1016/0005-2728(87)90136-8. DOI

Shen J.R., Inoue Y. Binding and functional properties of two new extrinsic components, cytochrome c-550 and a 12-kDa protein, in cyanobacterial photosystem II. Biochemistry. 1993;32:1825–1832. doi: 10.1021/bi00058a017. PubMed DOI

Shen J.R., Kamiya N. Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. Biochemistry. 2000;39:14739–14744. doi: 10.1021/bi001402m. PubMed DOI

Kawakami K., Shen J.R. Purification of fully active and crystallizable photosystem II from thermophilic cyanobacteria. Methods Enzymol. 2018;613:1–16. doi: 10.1016/bs.mie.2018.10.002. PubMed DOI

Schreiber U., Krieger A. Two fundamentally different types of variable chlorophyll fluorescence in vivo. FEBS Lett. 1996;397:131–135. doi: 10.1016/S0014-5793(96)01176-3. PubMed DOI

Allen J.P., Chamberlain K.D., Williams J.C. Identification of amino acid residues in a proton release pathway near the bacteriochlorophyll dimer in reaction centers from Rhodobacter sphaeroides. Photosynth. Res. 2022:1–12. doi: 10.1007/s11120-022-00968-x. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...