[PDF] https://doi.org/10.3952/physics.v58i4.3881

Open access article / Atviros prieigos straipsnis
Lith. J. Phys. 58, 379–390 (2018)
 

FLUCTUATING ANTENNA MODEL: APPLICATIONS AND PROSPECTS
  Gediminas Trinkūnasa and Jevgenij Chmeliova,b
 aDepartment of Molecular Compound Physics, Center for Physical Sciences and Technology, Saulėtekio 3, 10257 Vilnius, Lithuania
bInstitute of Chemical Physics, Faculty of Physics, Vilnius University, Saulėtekio 9, 10222 Vilnius, Lithuania
 E-mail: gediminas.trinkunas@ftmc.lt
Received 11 December 2018; accepted 2 January 2019

Recently, we proposed a simple conceptual fluctuating antenna model (FAM), describing excitation diffusion and trapping in a continuous medium, where variations of the excitation transfer pathways are taken into account by the introduced fractional space dimension. Since then, this model has been successfully applied to simulate multi-exponential excitation quenching kinetics in a series of plant photosynthetic systems, purified from the thylakoid membranes, without invoking a radical pair state in the reaction centre. Here, we overview this model and its parameters obtained for various systems, and extend the  area of its applications to several pigment–protein supercomplexes containing the photosystem I (PSI). We show that while the diffusion in the PSI core is virtually three-dimensional, the PSI core aggregates interconnected with other light-harvesting complexes (LHCI and/or LHCII) are characterized by a substantially reduced dimension, which indicates a smaller number of energy transfer links from LHCI to the PSI core. We also suggest that in vivo both PSI and PSII antennae are substantially larger than those observed in the isolated systems: PSII antenna contains in total about 6 LHCII trimers while PSI is aggregated with at least one LHCII trimer. The obtained results show that FAM can be a very useful tool to follow photosynthetic apparatus transformations during short- and long-term adaptation to varying light, monitored by kinetic fluorescence spectroscopy.
Keywords: time-resolved fluorescence, decay associated spectra, ligh-harvesting complex
PACS: 87.15.A-, 31.70.Hq, 71.35.-y, 78.47.D-

FLIUKTUOJANČIOSIOS ANTENOS MODELIS: TAIKYMAI IR PERSPEKTYVOS
Gediminas Trinkūnasa, Jevgenij Chmeliova,b

aFizinių ir technologijos mokslų centro Molekulinių darinių fizikos skyrius, Vilnius, Lietuva
bVilniaus universiteto Fizikos fakultetas, Vilnius, Lietuva
 
Neseniai buvo pasiūlytas paprastas konceptualus fliuktuojančiosios antenos modelis (FAM), apibūdinantis sužadinimo difuziją ir pagavimą tolydžioje terpėje bei atsižvelgiantis į kintančius sužadinimo pernašos kelius trupmenine erd­vės dimensija. Nuo FAM paskelbimo jis buvo sėkmingai pritaikytas modeliuojant neeksponentines sužadinimo gesimo kinetikas daugelyje augalų fotosintetinių sistemų neįvedant radikalų poros būsenų reakcijų centruose. Apžvelgiami gauti sistemų parametrai ir praplečiamos FAM taikymo sritys įvairioms pirmosios fotosistemos (PSI) dalelėms, kaip, pavyzdžiui, PSI kompleksui su pagrindiniu augalų šviesorankos kompleksu LHCII.
Parodoma, kad sužadinimo difuzija PSI branduolio komplekse yra beveik trimatė. PSI branduolio ir LHCI superkompleksui būdinga daug mažesnė dimensija, atspindinti minimalų energijos pernašos jungčių skaičių tarp LHCI ir PSI branduolio. FAM įvertinimai rodo, kad tiek PSI, tiek PSII antenos natūraliomis sąlygomis yra daug didesnės nei žinomose sistemose, ištrauktose iš tilakoidų membranų: PSII antenoje yra maždaug 6 LHCII trimerai, o PSI yra agreguota su bent vienu LHCII trimeru. Rezultatai rodo, kad remiantis kinetinės fluorescencijos spektroskopijos duomenimis, FAM gali būti labai naudingas siekiant stebėti fotosintetinių sistemų kaitą tiek trumpalaikiame, tiek ir ilgalaikiame prisitaikyme prie kintančios apšvitos.

References / Nuorodos

[1] R.E. Blankenship, Molecular Mechanisms of Photosynthesis, 2nd ed. (Wiley Blackwell, Chichester, 2014),
https://doi.org/ 10.1002/9780470758472
[2] E. Belgio, E. Kapitonova, J. Chmeliov, C.D.P. Duffy, P. Ungerer, L. Valkunas, and A.V. Ruban, Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps, Nat. Commun. 5, 4433 (2014),
https://doi.org/10.1038/ncomms5433
[3] S. Farooq, J. Chmeliov, E. Wientjes, R. Koehorst, A. Bader, L. Valkunas, G. Trinkunas, and H. van Amerongen, Dynamic feedback of the photosystem II reaction centre on photoprotection in plants, Nat. Plants 4(4), 225–231 (2018),
https://doi.org/10.1038/s41477-018-0127-8
[4] J. Kromdijk, K. Głowacka, L. Leonelli, S.T. Gabilly, M. Iwai, K.K. Niyogi, and S.P. Long, Improving photosynthesis and crop productivity by accelerating recovery from photoprotection, Science 354, 857–861 (2016),
https://doi.org/10.1126/science.aai8878
[5] C.D.P. Duffy, L. Valkunas, and A.V. Ruban, Light-harvesting processes in the dynamic photosynthetic antenna, Phys. Chem. Chem. Phys. 15(43), 18752–18770 (2013),
https://doi.org/10.1039/c3cp51878g
[6] J. Chmeliov, G. Trinkunas, H. van Amerongen, and L. Valkunas, Light harvesting in a fluctuating antenna, J. Am. Chem. Soc. 136(25), 8963–8972 (2014),
https://doi.org/10.1021/ja5027858
[7] K. Broess, G. Trinkunas, C.D. van der Weij-de Wit, J.P. Dekker, A. van Hoek, and H. van Amerongen, Excitation energy transfer and charge separation in photosystem II membranes revisited, Biophys. J. 91(10), 3776–3786 (2006),
https://doi.org/10.1529/biophysj.106.085068
[8] L. Valkunas, G. Trinkunas, J. Chmeliov, and A.V. Ruban, Modeling of exciton quenching in photosystem II, Phys. Chem. Chem. Phys. 11(35), 7576–7584 (2009),
https://doi.org/10.1039/b901848d
[9] S. Caffarri, K. Broess, R. Croce, and H. van Amerongen, Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes, Biophys. J. 100(9), 2094–2103 (2011),
https://doi.org/10.1016/j.bpj.2011.03.049
[10] D.I.G. Bennett, K. Amarnath, and G.R. Fleming, A structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes, J. Am. Chem. Soc. 135(24), 9164–9173 (2013),
https://doi.org/10.1021/ja403685a
[11] V.I. Novoderezhkin, M.A. Palacios, H. van Amerongen, and R. van Grondelle, Excitation dynamics in the LHCII complex of higher plants: Modeling based on the 2.72 Å crystal structure, J. Phys. Chem. B 109(20), 10493–10504 (2005),
https://doi.org/10.1021/jp044082f
[12] F. Müh, T. Renger, and A. Zouni, Crystal structure of cyanobacterial photosystem II at 3.0 Å resolution: A closer look at the antenna system and the small membrane-intrinsic subunits, Plant Physiol. Biochem. 46(3), 238–264 (2008),
https://doi.org/10.1016/j.plaphy.2008.01.003
[13] C.D.P. Duffy, L. Valkunas, and A.V. Ruban, Quantum mechanical calculations of xanthophyll–chlorophyll electronic coupling in the light-harvesting antenna of photosystem I of higher plants, J. Phys. Chem. B 117(25), 7605–7614 (2013),
https://doi.org/10.1021/jp4025848
[14] J. Chmeliov, W.P. Bricker, C. Lo, E. Jouin, L. Valkunas, A.V. Ruban, and C.D.P. Duffy, An 'all pigment' model of excitation quenching in LHCII, Phys. Chem. Chem. Phys. 17(24), 15857–15867 (2015),
https://doi.org/10.1039/C5CP01905B
[15] V. Barzda, V. Gulbinas, R. Kananavicius, V. Cervinskas, H. van Amerongen, R. van Grondelle, and L. Valkunas, Singlet–singlet annihilation kinetics in aggregates and trimers of LHCII, Biophys. J. 80(5), 2409–2421 (2001),
https://doi.org/10.1016/S0006-3495(01)76210-8
[16] S. Farooq, J. Chmeliov, G. Trinkunas, L. Valkunas, and H. van Amerongen, Is there excitation energy transfer between different layers of stacked photosystem-II-containing thylakoid membranes? J. Phys. Chem. Lett. 7(7), 1406–1410 (2016),
https://doi.org/10.1021/acs.jpclett.6b00474
[17] G. Garab, Self-assembly and structural–functional flexibility of oxygenic photosynthetic machineries: Personal perspectives, Photosynth. Res. 127, 131–150 (2016),
https://doi.org/10.1007/s11120-015-0192-z
[18] N.E. Holt, D. Zigmantas, L. Valkunas, X.P. Li, K.K. Niyogi, and G.R. Fleming, Carotenoid cation formation and the regulation of photosynthetic light harvesting, Science 307(5708), 433–436 (2005),
https://doi.org/10.1126/science.1105833
[19] A.A. Pascal, Z.F. Liu, K. Broess, B. van Oort, H. van Amerongen, C. Wang, P. Horton, B. Robert, W.R. Chang, and A. Ruban, Molecular basis of photoprotection and control of photosynthetic light-harvesting, Nature 436(7047), 134–137 (2005),
https://doi.org/10.1038/nature03795
[20] A.V. Ruban, R. Berera, C. Ilioaia, I.H.M. van Stokkum, J.T.M. Kennis, A.A. Pascal, H. van Amerongen, B. Robert, P. Horton, and R. van Grondelle, Identification of a mechanism of photoprotective energy dissipation in higher plants, Nature 450(7169), 575–578 (2007),
https://doi.org/10.1038/nature06262
[21] T.K. Ahn, T.J. Avenson, M. Ballottari, Y.C. Cheng, K.K. Niyogi, R. Bassi, and G.R. Fleming, Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein, Science 320(5877), 794–797 (2008),
https://doi.org/10.1126/science.1154800
[22] H. Staleva, J. Komenda, M.K. Shukla, V. Šlouf, R. Kaňa, T. Polívka, and R. Sobotka, Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins, Nat. Chem. Biol. 11(4), 287–291 (2015),
https://doi.org/10.1038/nchembio.1755
[23] J. Chmeliov, A. Gelzinis, E. Songaila, R. Augulis, C.D.P. Duffy, A.V. Ruban, and L. Valkunas, The nature of self-regulation in photosynthetic light-harvesting antenna, Nat. Plants 2, 16045 (2016),
https://doi.org/10.1038/nplants.2016.45
[24] J. Chmeliov, G. Trinkunas, H. van Amerongen, and L. Valkunas, Excitation migration in fluctuating light-harvesting antenna systems, Photosynth. Res. 127(1), 49–60 (2016),
https://doi.org/10.1007/s11120-015-0083-3
[25] M.G. Müller, P. Lambrev, M. Reus, E. Wientjes, R. Croce, and A.R. Holzwarth, Singlet energy dissipation in the photosystem II light-harvesting complex does not involve energy transfer to carotenoids, ChemPhysChem 11(6), 1289–1296 (2010),
https://doi.org/10.1002/cphc.200900852
[26] M. Mamedov, G.V. Nadtochenko, and A. Semenov, Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms, Photosynth. Res. 125, 51–63 (2015),
https://doi.org/10.1007/s11120-015-0088-y
[27] D.A. Cherepanov, G.E. Milanovsky, O.A. Gopta, R. Balasubramanian, D.A. Bryant, A.Y. Semenov, and J.H. Golbeck, Electron–phonon coupling in cyanobacterial photosystem I, J. Phys. Chem. B 122, 7943–7955 (2018),
https://doi.org/10.1021/acs.jpcb.8b03906
[28] R. Croce and H. van Amerongen, Light-harvest ing in photosystem I, Photosynth. Res. 116(2–3), 153–166 (2013),
https://doi.org/10.1007/s11120-013-9838-x
[29] I.H.M. van Stokkum, D.S. Larsen, and R. van Grondelle, Global and target analysis of time-resolved spectra, Biochim. Biophys. Acta 1657, 82–104 (2004),
https://doi.org/10.1016/j.bbabio.2004.04.011
[30] M. Brecht, V. Radics, J.B. Nieder, and R. Bittl, Protein dynamics-induced variation of excitation energy transfer pathways, Proc. Natl. Acad. Sci. U.S.A. 106(29), 11857–11861 (2009),
https://doi.org/10.1073/pnas.0903586106
[31] T.P.J. Krüger, E. Wientjes, R. Croce, and R. van Grondelle, Conformational switching explains the intrinsic multifunctionality of plant light-harvesting complexes, Proc. Natl. Acad. Sci. U.S.A. 108(33), 13516–13521 (2011),
https://doi.org/10.1073/pnas.1105411108
[32] T.P.J. Krüger, V.I. Novoderezkhin, C. Ilioaia, and R. van Grondelle, Fluorescence spectral dynamics of single LHCII trimers, Biophys. J. 98(12), 3093–3101 (2010),
https://doi.org/10.1016/j.bpj.2010.03.028
[33] I. Caspy and N. Nelson, Structure of the plant photosystem I, Biochem. Soc. Trans. 46, 285–294 (2018),
https://doi.org/10.1042/BST20170299
[34] S. Vaitekonis, G. Trinkunas, and L. Valkunas, Red chlorophylls in the exciton model of photosystem I, Photosynth. Res. 86, 185–201 (2005),
https://doi.org/10.1007/s11120-005-2747-x
[35] M.K. Sener, C. Jolley, A. Ben-Shem, P. Fromme, N. Nelson, R. Croce, and K. Schulten, Comparison of the light-harvesting networks of plant and cyanobacterial photosystem I, Biophys. J. 89, 1630–1642 (2005),
https://doi.org/10.1529/biophysj.105.066464
[36] E. Wientjes, I.H.M. van Stokkum, H. van Amerongen, and R. Croce, The role of the individual Lhcas in photosystem I excitation energy trapping, Biophys. J. 101(3), 745–754 (2011),
https://doi.org/10.1016/j.bpj.2011.06.045
[37] E. Wientjes, H. van Amerongen, and R. Croce, LHCII is an antenna of both photosystems after long-term acclimation, Biochim. Biophys. Acta Bioenerg. 1827(3), 420–426 (2013),
https://doi.org/10.1016/j.bbabio.2012.12.009
[38] E. Molotokaite, W. Remelli, A.P. Casazza, G. Zucchelli, D. Polli, G. Cerullo, and S. Santabarbara, Trapping dynamics in photosystem I-light harvesting complex I of higher plants is governed by the competition between excited state diffusion from low energy states and photochemical charge separation, J. Phys. Chem. B 121, 9816–9830 (2017),
https://doi.org/10.1021/acs.jpcb.7b07064
[39] T.P. Causgrove, S. Yang, and W.S. Struve, Polarized pump-probe spectroscopy of photosystem I antenna excitation transport, J. Phys. Chem. 93(18), 6844–6850 (1989),
https://doi.org/10.1021/j100355a053
[40] S. Savikhin, W. Xu, P.R. Chitnis, and W.S. Struve, Ultrafast primary processes in PSI from Synechocystis sp. PCC 6803: Roles of P700 and A(0), Biophys. J. 79, 1573–1586 (2000),
https://doi.org/10.1016/S0006-3495(00)76408-3
[41] C. Slavov, M. Ballottari, T. Morosinotto, R. Bassi, and A.R. Holzwarth, Trap-limited charge separation kinetics in higher plant photosystem I complexes, Biophys. J. 94, 3601–3612 (2008),
https://doi.org/10.1529/biophysj.107.117101
[42] B. van Oort, M. Alberts, S. de Bianchi, L. Dall'Osto, R. Bassi, G. Trinkunas, R. Croce, and H. van Amerongen, Effect of antenna-depletion in photosystem II on excitation energy transfer in Arabidopsis thaliana, Biophys. J. 98(5), 922–931 (2010),
https://doi.org/10.1016/j.bpj.2009.11.012
[43] R.C. Jennings, G. Zucchelli, R. Croce, and F.M. Garlaschi, The photochemical trapping rate from red spectral states in PSI–LHCI is determined by thermal activation of energy transfer to bulk chlorophylls, Biochim. Biophys. Acta Bioenerg. 1557, 91–98 (2003),
https://doi.org/10.1016/S0005-2728(02)00399-7
[44] S. Vassiliev, C.-I. Lee, G.W. Brudvig, and D. Bruce, Structure-based kinetic modeling of excited-state transfer and trapping in histidine-tagged photosystem II core complexes from Synechocystis, Biochemistry 41(40), 12236–12243 (2002),
https://doi.org/10.1021/bi0262597
[45] E.G. Andrizhiyevskaya, D. Frolov, R. van Grondelle, and J.P. Dekker, On the role of the CP47 core antenna in the energy transfer and trapping dynamics of photosystem II, Phys. Chem. Chem. Phys. 6(20), 4810–4819 (2004),
https://doi.org/10.1039/b411977k
[46] M.L. Groot, N.P. Pawlowicz, L.J.G.W. van Wilderen, J. Breton, I.H.M. van Stokkum, and R. van Grondelle, Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 102(37), 13087–13092 (2005),
https://doi.org/10.1073/pnas.0503483102
[47] Y. Miloslavina, M. Szczepaniak, M.G. Müller, J. Sander, M. Nowaczyk, M. Rögner, and A.R. Holzwarth, Charge separation kinetics in intact photosystem II core particles is trap-limited. A picosecond fluorescence study, Biochemistry 45(7), 2436–2442 (2006),
https://doi.org/10.1021/bi052248c
[48] K. Broess, G. Trinkunas, A. van Hoek, R. Croce, and H. van Amerongen, Determination of the excitation migration time in photosystem II – consequences for the membrane organization and charge separation parameters, Biochim. Biophys. Acta Bioenerg. 1777(5), 404–409 (2008),
https://doi.org/10.1016/j.bbabio.2008.02.003
[49] K. Amarnath, D.I.G. Bennett, A.R. Schneider, and G.R. Fleming, Multiscale model of light harvesting by photosystem II in plants, Proc. Natl. Acad. Sci. U.S.A. 113, 1156–1161 (2016),
https://doi.org/10.1073/pnas.1524999113
[50] D.I.G. Bennett, G.R. Fleming, and K. Amarnath, Energy-dependent quenching adjusts the excitation diffusion length to regulate photosynthetic light harvesting, Proc. Natl. Acad. Sci. U.S.A. 115, E9523–E9531 (2018),
https://doi.org/10.1073/pnas.1806597115
[51] C.D. van der Weij-de Wit, J.P. Dekker, R. van Grondelle, and I.H.M. van Stokkum, Charge separation is virtually irreversible in photosystem II core complexes with oxidized primary quinone acceptor, J. Phys. Chem. A 115(16), 3947–3956 (2011),
https://doi.org/10.1021/jp1083746