Abstract
This study aimed to clarify (1) which pigment in a photosystem II (PSII) core complex is responsible for the 695-nm emission at 77 K and (2) the molecular basis for the oxidation-induced fluorescence quenching in PSII. Picosecond time-resolved fluorescence dynamics was compared between the dimeric and monomeric PSII with and without addition of an oxidant. The results indicated that the excitation-energy flow to the 695-nm-emitting chlorophyll (Chl) at 36 K and 77 K was hindered upon monomerization, clearly demonstrating significant exciton migration from the Chls on one monomer to the 695-nm-emitting pigment on the adjacent monomer. Oxidation of the redox-active Chl, which is named ChlZ caused almost equal quenching of the 684-nm and 695-nm emission bands in the dimer, and lower quenching of the 695-nm band in the monomer. These results suggested two possible scenarios responsible for the 695-nm emission band: (A) Chl11-13 pair and the oxidized ChlZD1 work as the 695-nm emitting Chl and the quenching site, respectively, and (B) Chl29 and the oxidized ChlZD2 work as the 695-nm emitting Chl and the quenching site, respectively.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Byrdin M, Jordan P, Krauss N, Fromme P, Stehlik D, Schlodder E (2002) Light harvesting in photosystem I: modeling based on the 2.5-Å structure of photosystem i from Synechococcus elongatus. Biophys J 83:433–457
Chen JH, Kell A, Acharya K, Kupitz C, Fromme P, Jankowiak R (2015) Critical assessment of the emission spectra of various photosystem II core complexes. Photosynth Res 124(3):253–265. https://doi.org/10.1007/s11120-015-0128-7
D’Haene SE, Sobotka R, Bučinská L, Dekker JP (1847) Komenda J (2015) interaction of the PsbH subunit with a chlorophyll bound to histidine 114 of CP47 is responsible for the red 77 K fluorescence of Photosystem II. Biochim Biophys Acta 10:1327–1334. https://doi.org/10.1016/j.bbabio.2015.07.003
Damjanović A, Vaswani HM, Fromme P, Fleming GR (2002) Chlorophyll excitations in photosystem I of Synechococcus elongatus. J Phys Chem B 106:10251–10262
Davis MS, Forman A, Fajer J (1979) Ligated chlorophyll cation radicals—their function in photosystem-II of plant photosynthesis. Proc Natl Acad Sci USA 76(9):4170–4174
de Paula JC, Innes JB, Brudvig GW (1985) Electron transfer in photosystem II at cryogenic temperatures. Biochem Us 24(27):8114–8120. https://doi.org/10.1021/Bi00348a042
de Weerd FL, Palacios MA, Andrizhiyevskaya EG, Dekker JP, van Grondelle R (2002) Identifying the lowest electronic states of the chlorophylls in the CP47 core antenna protein of photosystem II. Biochem Us 41(51):15224–15233. https://doi.org/10.1021/bi0261948
Deinum G, Aartsma TJ, van Grondelle R, Amesz J (1989) Singlet-singlet excitation annihilation measurements on the antenna of Rhodospirillum rubrum between 300 and 4-K. Biochim Biophys Acta 976(1):63–69. https://doi.org/10.1016/S0005-2728(89)80189-6
Folea IM, Zhang P, Aro EM, Boekema EJ (2008) Domain organization of photosystem II in membranes of the cyanobacterium Synechocystis PCC6803 investigated by electron microscopy. Febs Lett 582(12):1749–1754. https://doi.org/10.1016/j.febslet.2008.04.044
Groot ML, Pawlowicz NP, van Wilderen LJGW, Breton J, van Stokkum IHM, van Grondelle R (2005) Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc Natl Acad Sci USA 102(37):13087–13092. https://doi.org/10.1073/pnas.0503483102
Groot ML, Peterman EJG, van Stokkum IHM, Dekker JP, van Grondelle R (1995) Triplet and fluorescing states of the Cp47 antenna complex of photosystem-II studied as a function of temperature. Biophys J 68(1):281–290
Hall J, Renger T, Müh F, Picorel R, Krausz E (2016) The lowest-energy chlorophyll of photosystem II is adjacent to the peripheral antenna: emitting states of CP47 assigned via circularly polarized luminescence. Biochim Biophys Acta 9:1580–1593. https://doi.org/10.1016/j.bbabio.2016.06.007
Heber U, Bilger W, Shuvalov VA (2006) Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation. J Exp Bot 57(12):2993–3006. https://doi.org/10.1093/jxb/erl058
Jassas M, Reinot T, Kell A, Jankowiak R (2017) Toward an understanding of the excitonic structure of the CP47 antenna protein complex of photosystem II revealed via circularly polarized luminescence. J Phys Chem B 121(17):4364–4378. https://doi.org/10.1021/acs.jpcb.7b00362
Kaminskaya O, Kern J, Shuvalov VA, Renger G (2005) Extinction coefficients of cytochromes b559 and c550 of Thermosynechococus elongatus and Cyt b559/PS II stoichiometry of higher plants. Biochim Biophys Acta 1708(3):333–341. https://doi.org/10.1016/j.bbabio.2005.05.002
Kaucikas M, Maghlaoui K, Barber J, Renger T, van Thor JJ (2016) Ultrafast infrared observation of exciton equilibration from oriented single crystals of photosystem II. Nat Commun. https://doi.org/10.1038/Ncomms13977
Kitajima Y, Noguchi T (2006) Photooxidation pathway of chlorophyll Z in photosystem II as studied by Fourier transform infrared spectroscopy. Biochem-Us 45(6):1938–1945. https://doi.org/10.1021/bi052346y
Komura M, Shibata Y, Itoh S (2006) A new fluorescence band F689 in photosystem II revealed by picosecond analysis at 4–77 K: function of two terminal energy sinks F689 and F695 in PS II. Biochim Biophys Acta 1757(12):1657–1668. https://doi.org/10.1016/j.bbabio.2006.09.007
Kosuge K, Tokutsu R, Kim E, Akimoto S, Yokono M, Ueno Y, Minagawa J (2018) LHCSR1-dependent fluorescence quenching is mediated by excitation energy transfer from LHCII to photosystem I in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 115(14):3722–3727. https://doi.org/10.1073/pnas.1720574115
Liu HJ, Zhang H, Niedzwiedzki DM, Prado M, He GN, Gross ML, Blankenship RE (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342(6162):1104–1107. https://doi.org/10.1126/science.1242321
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 30 angstrom resolution structure of photosystem II. Nature 438(7070):1040–1044. https://doi.org/10.1038/nature04224
Müh F, Plöckinger M, Ortmayer H, Busch MSA, Lindorfer D, Adolphs J, Renger T (2015) The quest for energy traps in the CP43 antenna of photosystem II. J Photoch Photobio B 152:286–300. https://doi.org/10.1016/j.jphotobiol.2015.05.023
Müh F, Zouni A (2020) Structural basis of light-harvesting in the photosystem II core complex. Protein Sci 29(5):1090–1119. https://doi.org/10.1002/pro.3841
Mohamed A, Nagao R, Noguchi T, Fukumura H, Shibata Y (2016) Structure-based modeling of fluorescence kinetics of photosystem II: relation between its dimeric form and photoregulation. J Phys Chem B 120(3):365–376. https://doi.org/10.1021/acs.jpcb.5b09103
Najafpour MM, Renger G, Holyńska M, Moghaddam AN, Aro EM, Carpentier R, Nishihara H, Eaton-Rye JJ, Shen J-R, Allakhverdiev SI (2016) Manganese compounds as water-oxidizing catalysts: from the natural water-oxidizing complex to nanosized manganese oxide structures. Chem Rev 116(5):2886–2936. https://doi.org/10.1021/acs.chemrev.5b00340
Neupane B, Dang NC, Acharya K, Reppert M, Zazubovich V, Picorel R, Seibert M, Jankowiak R (2010) Insight into the electronic structure of the CP47 antenna protein complex of photosystem ii: hole burning and fluorescence study. J Am Chem Soc 132(12):4214–4229. https://doi.org/10.1021/Ja908510w
Nicol L, Nawrocki WJ, Croce R (2019) Disentangling the sites of non-photochemical quenching in vascular plants. Nat Plants 5(11):1177. https://doi.org/10.1038/s41477-019-0526-5
Raszewski G, Renger T (2008) Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J Am Chem Soc 130(13):4431–4446. https://doi.org/10.1021/ja7099826
Reinot T, Chen J, Kell A, Jassas M, Robben KC, Zazubovich V, Jankowiak R (2016) On the conflicting estimations of pigment site energies in photosynthetic complexes: a case study of the CP47 complex. Anal Chem Insights 11:35–48
Reppert M, Acharya K, Neupane B, Jankowiak R (2010) Lowest electronic states of the CP47 antenna protein complex of photosystem II: simulation of optical spectra and revised structural assignmentst. J Phys Chem B 114(36):11884–11898. https://doi.org/10.1021/jp103995h
Sakai Y, Hirayama S (1988) A fast deconvolution method to analyze fluorescence decays when the excitation pulse repetition period is less than the decay times. J Lumin 39(3):145–151. https://doi.org/10.1016/0022-2313(88)90069-5
Schatz GH, Brock H, Holzwarth AR (1987) Picosecond kinetics of fluorescence and absorbency changes in photosystem-II particles excited at low photon density. P Natl Acad Sci USA 84(23):8414–8418. https://doi.org/10.1073/pnas.84.23.8414
Schlodder E, Renger T, Raszewski G, Coleman WJ, Nixon PJ, Cohen RO, Diner BA (2008) Site-directed mutations at D1-Thr179 of photosystem II in Synechocystis sp PCC 6803 modify the spectroscopic properties of the accessory chlorophyll in the D1-branch of the reaction center. Biochemi-Us 47(10):3143–3154. https://doi.org/10.1021/bi702059f
Schweitzer RH, Melkozernov AN, Blankenship RE, Brudvig GW (1998) Time-resolved fluorescence measurements of photosystem-II: the effect of quenching by oxidized chlorophyll Z. J Phys Chem B 102(42):8320–8326
Shen J-R (2015) The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu Rev Plant Biol 66:23–48. https://doi.org/10.1146/annurev-arplant-050312-120129
Shen J-R, Kawakami K, Koike H (2011) Purification and crystallization of oxygen-evolving photosystem II core complex from thermophilic cyanobacteria. In: Carpentier R. (eds) Photosynthesis research protocols. Methods in molecular biology. vol 684. doi:https://doi.org/10.1007/978-1-60761-925-3_5
Shibata Y, Nishi S, Kawakami K, Shen J-R, Renger T (2013) Photosystem II does not possess a simple excitation energy funnel: time-resolved fluorescence spectroscopy meets theory. J Am Chem Soc 135(18):6903–6914. https://doi.org/10.1021/ja312586p
Sirohiwal A, Neese F, Pantazis DA (2021) Chlorophyll excitation energies and structural stability of the CP47 antenna of photosystem II: a case study in the first-principles simulation of light-harvesting complexes. Chem Sci. https://doi.org/10.1039/d0sc06616h
Skandary S, Müh F, Ashraf I, Ibrahim M, Metzger M, Zouni A, Meixnera AJ, Brecht M (2017) Role of missing carotenoid in reducing the fluorescence of single monomeric photosystem II core complexes. Phys Chem Chem Phys 19:13189–13194
Suga M, Akita F, Yamashita K, Nakajima Y, Ueno G, Li HJ, Yamane T, Hirata K, Umena Y, Yonekura S, Yu LJ, Murakami H, Nomura T, Kimura T, Kubo M, Baba S, Kumasaka T, Tono K, Yabashi M, Isobe H, Yamaguchi K, Yamamoto M, Ago H, Shen J-R (2019) An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser. Science 366(6463):334. https://doi.org/10.1126/science.aax6998
Tracewell CA, Cua A, Stewart DH, Bocian DF, Brudvig GW (2001) Characterization of carotenoid and chlorophyll photooxidation in photosystem II. Biochemis-Us 40(1):193–203. https://doi.org/10.1021/bi001992o
Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 19 angstrom. Nature 473(7345):55–60. https://doi.org/10.1038/nature09913
van der Weij-de Wit CD, Dekker JP, van Grondelle R, van Stokkum IHM (2011) Charge separation is virtually irreversible in photosystem II core complexes with oxidized primary quinone acceptor. J Phys Chem A 115(16):3947–3956. https://doi.org/10.1021/jp1083746
Wang J, Gosztola D, Ruffle SV, Hemann C, Seibert M, Wasielewski MR, Hille R, Gustafson TL, Sayre RT (2002) Functional asymmetry of photosystem II D1 and D2 peripheral chlorophyll mutants of Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 99(6):4091–4096. https://doi.org/10.1073/pnas.062056899
Yamakawa H, Fukushima Y, Itoh S, Heber U (2012) Three different mechanisms of energy dissipation of a desiccation-tolerant moss serve one common purpose: to protect reaction centres against photo-oxidation. J Exp Bot 63(10):3765–3775. https://doi.org/10.1093/jxb/ers062
Yokono M, Takabayashi A, Akimoto S, Tanaka A (2015) A megacomplex composed of both photosystem reaction centres in higher plants. Nat Commun. https://doi.org/10.1038/Ncomms7675
Yokono M, Takabayashi A, Kishimoto J, Fujita T, Iwai M, Murakami A, Akimoto S, Tanaka A (2019) The PSI-PSII megacomplex in green plants. Plant Cell Physiol 60(5):1098–1108. https://doi.org/10.1093/pcp/pcz026
Yoneda Y, Katayama T, Nagasawa Y, Miyasaka H, Umena Y (2016) Dynamics of excitation energy transfer between the subunits of photosystem II dimer. J Am Chem Soc 138(36):11599–11605. https://doi.org/10.1021/jacs.6b04316
Zhang L, Silva DA, Zhang HD, Yue A, Yan YJ, Huang XH (2014) Dynamic protein conformations preferentially drive energy transfer along the active chain of the photosystem II reaction centre. Nat Commun 5:4170. https://doi.org/10.1038/Ncomms5170
Acknowledgements
This work was supported in part by JSPS KAKENHI Grant Number JP15H04356 to Y.S., 20K06684 to S.I., and JP22H04916 to J.-R. S.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mohamed, A., Nishi, S., Kawakami, K. et al. Exciton quenching by oxidized chlorophyll Z across the two adjacent monomers in a photosystem II core dimer. Photosynth Res 154, 277–289 (2022). https://doi.org/10.1007/s11120-022-00948-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-022-00948-1