Abstract
A widely discussed explanation for the prevalence of pairs or clusters of closely spaced electronic chromophores in photosynthetic light-harvesting proteins is the presence of ultrafast and highly directional excitation energy transfer pathways mediated by vibronic excitons, the delocalized optical excitations derived from mixing of the electronic and vibrational states of the chromophores. We discuss herein the hypothesis that internal conversion processes between exciton states on the <100 fs timescale are possible when the excitonic potential energy surfaces are controlled by the vibrational modes that induce charge transfer character in a strongly coupled system of chromophores. We discuss two examples, the peridinin–chlorophyll protein from marine dinoflagellates and the intact phycobilisome from cyanobacteria, in which the intramolecular charge-transfer (ICT) character arising from out-of-plane distortion of the conjugation of carotenoid or bilin chromophores also results in localization of the initially delocalized optical excitation on the vibrational timescale. Tuning of the ground state conformations of the chromophores to manipulate their ICT character provides a natural photoregulatory mechanism, which would control the overall quantum yield of excitation energy transfer by turning on and off the delocalized character of the optical excitations.
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References
Abramavicius D, Palmieri B, Voronine DV et al (2009) Coherent multidimensional optical spectroscopy of excitons in molecular aggregates; quasiparticle versus supermolecule perspectives. Chem Rev 109(6):2350–2408. https://doi.org/10.1021/cr800268n
Adir N (2005) Elucidation of the molecular structures of components of the phycobilisome: reconstructing a giant. Photosynth Res 85(1):15–32. https://doi.org/10.1007/s11120-004-2143-y
Allen JP, Feher G, Yeates TO et al (1986) Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by X-ray diffraction. Proc Natl Acad Sci USA 83:8589–8593
Anna JM, Scholes GD, van Grondelle R (2014) A little coherence in photosynthetic light harvesting. Bioscience 64(1):14–25. https://doi.org/10.1093/biosci/bit002
Atchity GJ, Xantheas SS, Ruedenberg K (1991) Potential energy surfaces near intersections. J Chem Phys 95(3):1862–1876. https://doi.org/10.1063/1.461036
Bandara S, Rockwell NC, Zeng X et al (2021) Crystal structure of a far-red-sensing cyanobacteriochrome reveals an atypical bilin conformation and spectral tuning mechanism. Proc Natl Acad Sci USA. https://doi.org/10.1073/pnas.2025094118
Bautista JA, Hiller RG, Sharples FP et al (1999) Singlet and triplet energy transfer in the peridinin-chlorophyll a-protein from Amphidinium carterae. J Phys Chem A 103(14):2267–2273. https://doi.org/10.1021/jp983943f
Beck WF, Bishop MM, Roscioli JD et al (2015) Excited state conformational dynamics in carotenoids: dark intermediates and excitation energy transfer. Arch Biochem Biophys 572:175–183. https://doi.org/10.1016/j.abb.2015.02.016
Beddard GS, Porter G (1976) Concentration quenching in chlorophyll. Nature 260(5549):366–367. https://doi.org/10.1038/260366a0
Beenken WJD, Dahlbom M, Kjellberg P et al (2002) Potential surfaces and delocalization of excitons in dimers. J Chem Phys 117(12):5810–5820. https://doi.org/10.1063/1.1502647
Beljonne D, Curutchet C, Scholes GD et al (2009) Beyond Förster resonance energy transfer in biological and nanoscale systems. J Phys Chem B 113:6583. https://doi.org/10.1021/jp900708f
Bernardi F, Olivucci M, Robb MA (1996) Potential energy surface crossings in organic photochemistry. Chem Soc Rev 25(5):321–328. https://doi.org/10.1039/CS9962500321
Bonačić-Koutecký V, Bruckmann P, Hiberty P et al (1975) Sudden polarization in the zwitterionic Z1 excited states of organic intermediates photochemical implications. Angew Chem Int Ed 14(8):575–576. https://doi.org/10.1002/anie.197505751
Bonačić-Koutecký V, Koutecký J, Michl J (1987) Neutral and charged biradicals, zwitterions, funnels in \(\text{ S}_{1}\), and proton translocation: their role in photochemistry, photophysics, and vision. Angew Chem Int Ed Engl 26(3):170–189. https://doi.org/10.1002/anie.198701701
Brejc K, Ficner R, Huber R et al (1995) Isolation, crystallization, crystal structure analysis and refinement of allophycocyanin from the cyanobacterium Spirulina platensis at 2.3 Å resolution. J Mol Biol 249(2):424–440. https://doi.org/10.1006/jmbi.1995.0307
Butkus V, Zigmantas D, Valkunas L et al (2012) Vibrational vs. electronic coherences in 2D spectrum of molecular systems. Chem Phys Lett 545:40–43. https://doi.org/10.1016/j.cplett.2012.07.014
Butkus V, Zigmantas D, Abramavicius D et al (2013) Distinctive character of electronic and vibrational coherences in disordered molecular aggregates. Chem Phys Lett 587:93–98. https://doi.org/10.1016/j.cplett.2013.09.043
Butkus V, Alster J, Bašinskaitė E et al (2017) Discrimination of diverse coherences allows identification of electronic transitions of a molecular nanoring. J Phys Chem Lett 8(10):2344–2349. https://doi.org/10.1021/acs.jpclett.7b00612
Camara-Artigas A, Blankenship RE, Allen JP (2003) The structure of the FMO protein from Chlorobium tepidum at 2.2 Å resolution. Photosynth Res 75(1):49–55. https://doi.org/10.1023/A:1022406703110
Cantor CR, Schimmel PR (1980) Biophysical chemistry part II: techniques for the study of biological structure and function. W. H, Freeman and Company, San Francisco
Cao J, Cogdell RJ, Coker DF et al (2020) Quantum biology revisited. Sci Adv 6(14):2375–2548. https://doi.org/10.1126/sciadv.aaz4888
Caram JR, Lewis NHC, Fidler AF et al (2012) Signatures of correlated excitonic dynamics in two-dimensional spectroscopy of the Fenna-Matthews-Olson photosynthetic complex. J Chem Phys 136(10):104505. https://doi.org/10.1063/1.3690498
Cerullo G, Polli D, Lanzani G et al (2002) Photosynthetic light harvesting by carotenoids: detection of an intermediate excited state. Science 298(5602):2395–2398. https://doi.org/10.1126/science.1074685
Chenu A, Scholes GD (2015) Coherence in energy transfer and photosynthesis. Annu Rev Phys Chem 66:69–96. https://doi.org/10.1146/annurev-physchem-040214-121713
Chin AW, Huelga SF, Plenio MB (2012) Coherence and decoherence in biological systems: principles of noise-assisted transport and the origin of long-lived coherences. Philos Trans A Math Phys Eng Sci 370(1972):3638–3657. https://doi.org/10.1098/rsta.2011.0224
Chin AW, Prior J, Rosenbach R et al (2013) The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment-protein complexes. Nat Phys 9(2):113. https://doi.org/10.1038/nphys2515
Christensson N, Kauffmann HF, Pullerits T et al (2012) Origin of long-lived coherences in light-harvesting complexes. J Phys Chem B 116(25):7449–7454. https://doi.org/10.1021/jp304649c
Chukhutsina VU, Baxter JM, Fadini A et al (2022) Light activation of orange carotenoid protein reveals bicycle-pedal single-bond isomerization. Nat Commun 13(1):6420. https://doi.org/10.1038/s41467-022-34137-4
Czarnecki K, Diers JR, Chynwat V et al (1997) Characterization of the strongly coupled, low-frequency vibrational modes of the special pair of photosynthetic reaction centers via isotopic labeling of the cofactors. J Am Chem Soc 119(2):415–426. https://doi.org/10.1021/ja963281c
Dahlbom M, Beenken W, Sundström V et al (2002) Collective excitation dynamics and polaron formation in molecular aggregates. Chem Phys Lett 364(5):556–561. https://doi.org/10.1016/S0009-2614(02)01372-6
de Weerd FL, van Stokkum IHM, van Grondelle R (2002) Subpicosecond dynamics in the excited state absorption of all-trans-\(\beta\)-carotene. Chem Phys Lett 354:38–43. https://doi.org/10.1016/S0009-2614(02)00095-7
Degli Esposti M, Crimi M, Körtner C et al (1991) The structure of the dihaem cytochrome b of fumarate reductase in Wolinella succinogenes: circular dichroism and sequence analysis studies. Biochim Biophys Acta 1056(3):243–249. https://doi.org/10.1016/s0005-2728(05)80055-6
Deisenhofer J, Michel H (1989) The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. Science 245:1463–1473. https://doi.org/10.1126/science.245.4925.1463
Deisenhofer J, Epp O, Miki K et al (1984) X-ray structure analysis of a membrane protein complex electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180(2):385–398. https://doi.org/10.1016/s0022-2836(84)80011-x
Deisenhofer J, Epp O, Miki K et al (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3.1 Å resolution. Nature 318:618–624. https://doi.org/10.1038/318618a0
Dijkstra AG, Wang C, Cao J et al (2015) Coherent exciton dynamics in the presence of underdamped vibrations. J Phys Chem Lett 6:627–632. https://doi.org/10.1021/jz502701u
Domínguez-Martín MA, Sauer PV, Kirst H et al (2022) Structures of a phycobilisome in light-harvesting and photoprotected states. Nature 609(7928):835–845. https://doi.org/10.1038/s41586-022-05156-4
Duan HG, Miller RJD, Thorwart M (2016) Impact of vibrational coherence on the quantum yield at a conical intersection. J Phys Chem Lett 7(17):3491–3496. https://doi.org/10.1021/acs.jpclett.6b01551
Duan HG, Prokhorenko VI, Cogdell RJ et al (2017) Nature does not rely on long-lived electronic quantum coherence for photosynthetic energy transfer. Proc Natl Acad Sci USA 114(32):8493–8498. https://doi.org/10.1073/pnas.1702261114
Duerring M, Schmidt GB, Huber R (1991) Isolation, crystallization, crystal structure analysis and refinement of constitutive C-phycocyanin from the chromatically adapting cyanobacterium Fremyella diplosiphon at 1.66 Å resolution. J Mol Biol 217(3):577–592. https://doi.org/10.1016/0022-2836(91)90759-Y
Edington MD, Riter RE, Beck WF (1995) Evidence for coherent energy transfer in allophycocyanin trimers. J Phys Chem 99(43):15699–15704. https://doi.org/10.1021/j100043a001
Edington MD, Riter RE, Beck WF (1996) Interexciton-state relaxation and exciton localization in allophycocyanin trimers. J Phys Chem 100(33):14206–14217. https://doi.org/10.1021/jp960454b
Edington MD, Riter RE, Beck WF (1997) Femtosecond transient hole-burning detection of interexciton-state radiationless decay in allophycocyanin trimers. J Phys Chem B 101(22):4473–4477. https://doi.org/10.1021/jp970424o
Engel GS, Calhoun TR, Read EL et al (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782–786. https://doi.org/10.1038/nature05678
Fenna RE, Matthews BW (1975) Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola. Nature 258(5536):573–577. https://doi.org/10.1038/258573a0
Fidder H, Knoester J, Wiersma DA (1991) Optical properties of disordered molecular aggregates: a numerical study. J Chem Phys 95(11):7880–7890
Fleming GR, Cho M (1996) Chromophore-solvent dynamics. Annu Rev Phys Chem 47:109–134. https://doi.org/10.1146/annurev.physchem.47.1.109
Förster T (1948) Zwischenmolekulare energiewanderung und fluoreszenz. Ann Phys (Berlin) 2:55–75. https://doi.org/10.1002/andp.19484370105
Förster T (1965) Delocalized excitation and excitation transfer. In: Sinanoğlu O (ed) Modern quantum chemistry part III: action of light and organic crystals. Academic Press, New York, pp 93–137
Förster T (1967) Mechanisms of energy transfer. In: Florkin M, Stotz EH (eds) Comprehensive biochemistry. Elsevier, Amsterdam, pp 61–80
Fransted KA, Caram JR, Hayes D et al (2012) Two-dimensional electronic spectroscopy of bacteriochlorophyll a in solution: elucidating the coherence dynamics of the Fenna-Matthews-Olson complex using its chromophore as a control. J Chem Phys 137:125101. https://doi.org/10.1063/1.4752107
Friesner R, Wertheimer R (1982) Model for primary charge separation in reaction centers of photosynthetic bacteria. Proc Natl Acad Sci USA 79(6):2138–2142. https://doi.org/10.1073/pnas.79.6.2138
Fujihashi Y, Fleming GR, Ishizaki A (2015) Impact of environmentally induced fluctuations on quantum mechanically mixed electronic and vibrational pigment states in photosynthetic energy transfer and 2D electronic spectra. J Chem Phys 142(21):212403. https://doi.org/10.1063/1.4914302
Fuller FD, Pan J, Gelzinis A et al (2014) Vibronic coherence in oxygenic photosynthesis. Nat Chem 6:706. https://doi.org/10.1038/nchem.2005
Gantt E (1975) Phycobilisomes: light-harvesting pigment complexes. Bioscience 25(12):781–788. https://doi.org/10.2307/1297221
Ghosh S, Bishop MM, Roscioli JD et al (2015) Femtosecond heterodyne transient-grating studies of nonradiative decay of the \(\text{ S}_{2}\) (1\(^{1}\text{ B}_{u}^{+}\)) state of \(\beta\)-carotene: contributions from dark intermediates and double-quantum coherences. J Phys Chem B 119(47):14905–14924. https://doi.org/10.1021/acs.jpcb.5b09405
Ghosh S, Bishop MM, Roscioli JD et al (2016) Femtosecond heterodyne transient grating studies of nonradiative deactivation of the \(\text{ S}_{2}\) (\(1^{1}\text{ B}_{u}^{+}\)) state of peridinin: detection and spectroscopic assignment of an intermediate in the decay pathway. J Phys Chem B 120:3601–3614. https://doi.org/10.1021/acs.jpcb.5b12753
Ghosh S, Roscioli JD, Bishop MM et al (2016) Torsional dynamics and intramolecular charge transfer in the \(\text{ S}_{2}\) (1\(^{1}\text{ B}_{u}^{+}\)) excited state of peridinin: a mechanism for enhanced mid-visible light harvesting. J Phys Chem Lett 7(18):3621–3626. https://doi.org/10.1021/acs.jpclett.6b01642
Ghosh S, Bishop MM, Roscioli JD et al (2017) Excitation energy transfer by coherent and incoherent mechanisms in the peridinin-chlorophyll a protein. J Phys Chem Lett 8:463–469. https://doi.org/10.1021/acs.jpclett.6b02881
Ginsberg NS, Cheng YC, Fleming GR (2009) Two-dimensional electronic spectroscopy of molecular aggregates. Acc Chem Res 42(9):1352–1363. https://doi.org/10.1021/ar9001075
Gisriel CJ, Elias E, Shen G et al (2023) Structural comparison of allophycocyanin variants reveals the molecular basis for their spectral differences. Photosynth Res. https://doi.org/10.1007/s11120-023-01048-4
Glazer AN (1985) Light harvesting by phycobilisomes. Annu Rev Biophys Biophys Chem 14:47–77. https://doi.org/10.1146/annurev.bb.14.060185.000403
Glazer AN (1989) Light guides directional energy transfer in a photosynthetic antenna. J Biol Chem 264(1):1–4
Gozem S, Luk HL, Schapiro I et al (2017) Theory and simulation of the ultrafast double-bond isomerization of biological chromophores. Chem Rev 117(22):13502–13565. https://doi.org/10.1021/acs.chemrev.7b00177
Guberman-Pfeffer MJ, Greco JA, Birge RR et al (2018) Light harvesting by equally contributing mechanisms in a photosynthetic antenna protein. J Phys Chem Lett 9(3):563–568. https://doi.org/10.1021/acs.jpclett.7b03211
Gurchiek JK, Rose JB, Guberman-Pfeffer MJ et al (2020) Fluorescence anisotropy detection of barrier crossing and ultrafast conformational dynamics in the \(\text{ S}_{2}\) state of \(\beta\)-carotene. J Phys Chem B 124(41):9029–9046. https://doi.org/10.1021/acs.jpcb.0c06961
Halpin A, Johnson PJ, Tempelaar R et al (2014) Two-dimensional spectroscopy of a molecular dimer unveils the effects of vibronic coupling on exciton coherences. Nat Chem 6(3):196–201. https://doi.org/10.1038/nchem.1834
Hayes D, Griffin GB, Engel GS (2013) Engineering coherence among excited states in synthetic heterodimer systems. Science 340(6139):1431–1434. https://doi.org/10.1126/science.1233828
Hein B, Kreisbeck C, Kramer T et al (2012) Modelling of oscillations in two-dimensional echo-spectra of the Fenna-Matthews-Olson complex. New J Phys 14(2):023018. https://doi.org/10.1088/1367-2630/14/2/023018
Hetherington CV, Mohan TMN, Tilluck RW et al (2023) Origin of vibronic coherences during carrier cooling in colloidal quantum dots. J Phys Chem Lett 14:11651–11658. https://doi.org/10.1021/acs.jpclett.3c02384
Hochstrasser RM, Kasha M (1964) Application of the exciton model to mono-molecular lamellar systems. Photochem Photobiol 3(4):317–331. https://doi.org/10.1111/j.1751-1097.1964.tb08155.x
Hoffman DP, Ellis SR, Mathies RA (2014) Characterization of a conical intersection in a charge-transfer dimer with two-dimensional time-resolved stimulated Raman spectroscopy. J Phys Chem A 118(27):4955–4965. https://doi.org/10.1021/jp5041986
Hofmann E, Wrench PM, Sharples FP et al (1996) Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science 272(5269):1788–1791. https://doi.org/10.1126/science.272.5269.1788
Holstein T (1959) Studies of polaron motion: Part I. the molecular-crystal model. Ann Phys 8(3):325–342. https://doi.org/10.1016/0003-4916(59)90002-8
Homoelle BJ, Edington MD, Diffey WM et al (1998) Stimulated photon-echo and transient-grating studies of protein-matrix solvation dynamics and interexciton-state radiationless decay in \(\alpha\) phycocyanin and allophycocyanin. J Phys Chem B 102:3044–3052. https://doi.org/10.1021/jp972782x
Huber H, Meyer M, Scheer H et al (1998) Temperature dependence of the primary electron transfer reaction in pigment-modified bacterial reaction centers. Photosynth Res 55(2):153–162. https://doi.org/10.1023/A:1006013613075
Ishizaki A, Fleming GR (2009) Unified treatment of quantum coherent and incoherent hopping dynamics in electronic energy transfer: reduced hierarchy equation approach. J Chem Phys 130(23):234111. https://doi.org/10.1063/1.3155372
Ishizaki A, Fleming GR (2012) Quantum coherence in photosynthetic light harvesting. Annu Rev Condens Matter Phys 3(1):333–361. https://doi.org/10.1146/annurev-conmatphys-020911-125126
Jean JM, Chan CK, Fleming GR (1988) Electronic energy transfer in photosynthetic bacterial reaction centers. Isr J Chem 28:169–175
Johnson SG, Small GJ (1991) Excited-state structure and energy-transfer dynamics of the bacteriochlorophyll a antenna complex from Prosthecochloris aestuarii. J Phys Chem 95(1):471–479. https://doi.org/10.1021/j100154a083
Johnson SG, Tang D, Jankowiak R et al (1989) Structure and marker mode of the primary electron donor state absorption of photosynthetic bacteria: hole-burned spectra. J Phys Chem 93(16):5953–5957. https://doi.org/10.1021/j100353a001
Johnson SG, Tang D, Jankowiak R et al (1990) Primary donor state mode structure and energy transfer in bacterial reaction centers. J Phys Chem 94(15):5849–5855. https://doi.org/10.1021/j100378a045
Jonas DM (2018) Vibrational and nonadiabatic coherence in 2D electronic spectroscopy, the Jahn-Teller effect, and energy transfer. Annu Rev Phys Chem 69(1):327–352. https://doi.org/10.1146/annurev-physchem-052516-050602
Jumper CC, Anna JM, Stradomska A et al (2014) Intramolecular radiationless transitions dominate exciton relaxation dynamics. Chem Phys Lett 599:23–33. https://doi.org/10.1016/j.cplett.2014.03.007
Kasha M (1963) Energy transfer mechanisms and the molecular exciton model for molecular aggregates. Radiat Res 20:55–70
Kim PW, Freer LH, Rockwell NC et al (2012) Femtosecond photodynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 1. Forward dynamics. Biochemistry 51(2):608–618. https://doi.org/10.1021/bi201507k
Kim PW, Freer LH, Rockwell NC et al (2012) Second-chance forward isomerization dynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. J Am Chem Soc 134(1):130–133. https://doi.org/10.1021/ja209533x
Kim PW, Pan J, Rockwell NC et al (2012) Ultrafast E to Z photoisomerization dynamics of the Cph1 phytochrome. Chem Phys Lett 549:86–92. https://doi.org/10.1016/j.cplett.2012.08.044
Klessinger M, Michl J (1995) Excited states and photochemistry of organic molecules. VCH Publishers, New York
Knapp EW, Scherer POJ, Fischer SF (1984) On the lineshapes of vibronically resolved molecular aggregate spectra. Application to pseudoisocyanin (PIC). Chem Phys Lett 111(4):481–486. https://doi.org/10.1016/0009-2614(84)85544-X
Knox RS (1975) Excitation energy transfer and migration: theoretical considerations. In: Govindjee (ed) Bioenergetics of photosynthesis. Academic Press, New York, pp 183–221
Kolli A, O’Reilly EJ, Scholes GD et al (2012) The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae. J Chem Phys 137(17):174109. https://doi.org/10.1063/1.4764100
Komiya H, Yeates TO, Rees DC et al (1988) Structure of the reaction center from Rhodopseudomonas sphaeroides R-26 and 2.4.1: symmetry relations and sequence comparisons between different species. Proc Natl Acad Sci USA 85:9012–9016
Kreisbeck C, Kramer T, Aspuru-Guzik A (2014) Scalable high-performance algorithm for the simulation of exciton dynamics. Application to the light-harvesting complex II in the presence of resonant vibrational modes. J Chem Theory Comput 10(9):4045–4054. https://doi.org/10.1021/ct500629s
Krüger TPJ, van Grondelle R, Gwizdala M (2019) The role of far-red spectral states in the energy regulation of phycobilisomes. Biochim Biophys Acta Bioenerg 4:341–349. https://doi.org/10.1016/j.bbabio.2019.01.007
Levine BG, Martínez TJ (2007) Isomerization through conical intersections. Annu Rev Phys Chem 58:613–634. https://doi.org/10.1146/annurev.physchem.57.032905.104612
Levine BG, Esch MP, Fales BS et al (2019) Conical intersections at the nanoscale: molecular ideas for materials. Annu Rev Phys Chem 70:21–43. https://doi.org/10.1146/annurev-physchem-042018-052425
Li YF, Zhou W, Blankenship RE et al (1997) Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. J Mol Biol 271(3):456–471. https://doi.org/10.1006/jmbi.1997.1189
Liu H, Zhang H, Niedzwiedzki DM et al (2013) Phycobilisomes supply excitations to both photosystems in a megacomplex in cyanobacteria. Science 342(6162):1104–1107. https://doi.org/10.1126/science.1242321
Maiuri M, Ostroumov EE, Saer RG et al (2018) Coherent wavepackets in the Fenna-Matthews-Olson complex are robust to excitonic-structure perturbations caused by mutagenesis. Nat Chem 10(2):177–183. https://doi.org/10.1038/nchem.2910
Malhado JP, Spezia R, Hynes JT (2011) Dynamical friction effects on the photoisomerization of a model protonated Schiff base in solution. J Phys Chem A 115:3720–3735. https://doi.org/10.1021/jp106096m
Malý P, Somsen OJG, Novoderezhkin VI et al (2016) The role of resonant vibrations in electronic energy transfer. Chemphyschem 17(9):1356–1368. https://doi.org/10.1002/cphc.201500965
Mančal T, Valkunas L, Fleming GR (2006) Theory of exciton-charge transfer state coupled systems. Chem Phys Lett 432(1):301–305. https://doi.org/10.1016/j.cplett.2006.10.055
Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811(3):265–322. https://doi.org/10.1016/0304-4173(85)90014-x
May V, Kühn O (2008) Charge and energy transfer dynamics in molecular systems. Wiley, Hoboken
McGregor A, Klartag M, David L et al (2008) Allophycocyanin trimer stability and functionality are primarily due to polar enhanced hydrophobicity of the phycocyanobilin binding pocket. J Mol Biol 384(2):406–421. https://doi.org/10.1016/j.jmb.2008.09.018
McRae EG (1963) Molecular vibrations in the exciton theory for molecular aggregates. IV. Excited states of weakly-coupled systems. Aust J Chem 16(3):295–314. https://doi.org/10.1071/ch9630295
Michl J (2004) Historical introduction. In: Domcke W, Yarkony D, Köppel H (eds) Conical intersections: electronic structure dynamics and spectroscopy. World Scientific, Singapore
Michl J, Bonačić-Koutecký V (1990) Electronic aspects of organic photochemistry. Wiley, New York
Mirkovic T, Ostroumov EE, Anna JM et al (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117(2):249–293. https://doi.org/10.1021/acs.chemrev.6b00002
Mohan TMN, Leslie CH, Sil S et al (2021) Broadband 2DES detection of vibrational coherence in the \(\text{ S}_{x}\) state of canthaxanthin. J Chem Phys 155(3):035103. https://doi.org/10.1063/5.0055598
Mukherjee S, Barbatti M (2022) Ultrafast internal conversion without energy crossing. Res Chem 4:100521. https://doi.org/10.1016/j.rechem.2022.100521
Myahkostupov M, Prusakova V, Oblinsky DG et al (2013) Structural refinement of ladder-type perylenediimide dimers: a classical tale of conformational dynamics. J Org Chem 78(17):8634–8644. https://doi.org/10.1021/jo401348w
Nalbach P, Mujica-Martinez CA, Thorwart M (2015) Vibronically coherent speed-up of the excitation energy transfer in the Fenna-Matthews-Olson complex. Phys Rev E Stat Nonlin Soft Matter Phys 91(2):022706. https://doi.org/10.1103/PhysRevE.91.022706
Niedringhaus A, Policht VR, Sechrist R et al (2018) Primary processes in the bacterial reaction center probed by two-dimensional electronic spectroscopy. Proc Natl Acad Sci USA 115(14):3563–3568. https://doi.org/10.1073/pnas.1721927115
Ohmae E, Fukumizu Y, Iwakura M et al (2005) Effects of mutation at methionine-42 of Escherichia coli dihydrofolate reductase on stability and function: implication of hydrophobic interactions. J Biochem 137(5):643–652. https://doi.org/10.1093/jb/mvi079
Ostroumov EE, Mulvaney RM, Anna JM et al (2013) Energy transfer pathways in light-harvesting complexes of purple bacteria as revealed by global kinetic analysis of two-dimensional transient spectra. J Phys Chem B 117(38):11349–11362. https://doi.org/10.1021/jp403028x
Ostroumov EE, Mulvaney RM, Cogdell RJ et al (2013) Broadband 2D electronic spectroscopy reveals a carotenoid dark state in purple bacteria. Science 340(6128):52–56. https://doi.org/10.1126/science.1230106
Panitchayangkoon G, Hayes D, Fransted KA et al (2010) Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc Natl Acad Sci USA 107(29):12766–12770. https://doi.org/10.1073/pnas.1005484107
Peng PP, Dong LL, Sun YF et al (2014) The structure of allophycocyanin b from Synechocystis PCC 6803 reveals the structural basis for the extreme redshift of the terminal emitter in phycobilisomes. Acta Crystallogr D Biol Crystallogr 70(Pt 10):2558–2569. https://doi.org/10.1107/S1399004714015776
Peters WK, Smith ER, Jonas DM (2011) Femtosecond pump-probe polarization spectroscopy of vibronic dynamics at conical intersections and funnels. In: Domcke W, Yarkony DR, Köppel H (eds) Conical intersections: theory, computation and experiment. World Scientific, New York, pp 715–745
Philipson KD, Sauer K (1973) Comparative study of the circular dichroism spectra of reaction centers from several photosynthetic bacteria. Biochemistry 12(3):535–539. https://doi.org/10.1021/bi00727a028
Philpott MR (1969) Theory of the vibrational structure of molecular excitons. Soluble one-phonon models. J Chem Phys 51(6):2616–2624
Policht VR, Niedringhaus A, Willow R et al (2022) Hidden vibronic and excitonic structure and vibronic coherence transfer in the bacterial reaction center. Sci Adv 8(1):eabk0953. https://doi.org/10.1126/sciadv.abk0953
Polívka T, Sundström V (2004) Ultrafast dynamics of carotenoid excited states-from solution to natural and artificial systems. Chem Rev 104(4):2021–2071. https://doi.org/10.1021/cr020674n
Polívka T, Sundström V (2009) Dark excited states of carotenoids: consensus and controversy. Chem Phys Lett 477:1–11. https://doi.org/10.1016/j.cplett.2009.06.011
Pollard WT, Mathies RA (1992) Analysis of femtosecond dynamic absorption spectra of nonstationary states. Annu Rev Phys Chem 43:497–523. https://doi.org/10.1146/annurev.pc.43.100192.002433
Pullerits T, Chachisvilis M, Jones MR et al (1994) Exciton dynamics in the light-harvesting complexes of Rhodobacter sphaeroides. Chem Phys Lett 224(3):355–365. https://doi.org/10.1016/0009-2614(94)00561-3
Rafiq S, Scholes GD (2019) From fundamental theories to quantum coherences in electron transfer. J Am Chem Soc 141(2):708–722. https://doi.org/10.1021/jacs.8b09059
Rashba ÉI (1966) Theory of vibronic spectra of molecular crystals. Sov J Exp Theor Phys 23:708
Renger T (2004) Theory of optical spectra involving charge transfer states: dynamic localization predicts a temperature dependent optical band shift. Phys Rev Lett 93(18):188101. https://doi.org/10.1103/PhysRevLett.93.188101
Riter RR, Edington MD, Beck WF (1996) Protein-matrix solvation dynamics in the \(\alpha\) subunit of C-phycocyanin. J Phys Chem 100(33):14198–14205. https://doi.org/10.1021/jp960453j
Riter RE, Edington MD, Beck WF (1997) Isolated-chromophore and exciton-state photophysics in C-phycocyanin trimers. J Phys Chem B 101(13):2366–2371. https://doi.org/10.1021/jp962609l
Romero E, Augulis R, Novoderezhkin VI et al (2014) Quantum coherence in photosynthesis for efficient solar energy conversion. Nat Phys 10(9):676–682. https://doi.org/10.1038/nphys3017
Roscioli JD, Ghosh S, LaFountain AM et al (2017) Quantum coherent excitation energy transfer by carotenoids in photosynthetic light harvesting. J Phys Chem Lett 8(20):5141–5147. https://doi.org/10.1021/acs.jpclett.7b01791
Roscioli JD, Ghosh S, LaFountain AM et al (2018) Structural tuning of quantum decoherence and coherent energy transfer in photosynthetic light harvesting. J Phys Chem Lett 9:5071–5077. https://doi.org/10.1021/acs.jpclett.8b01919
Rosinski J, Hainfeld JF, Rigbi M et al (1981) Phycobilisome ultrastructure and chromatic adaptation in Fremyella diplosiphon. Ann Bot 47(1):1–12. https://doi.org/10.1093/oxfordjournals.aob.a085984
Roth M, Lewit-Bentley A, Michel H et al (1989) Detergent structure in crystals of a bacterial photosynthetic reaction centre. Nature 340(6235):659–662. https://doi.org/10.1038/340659a0
Sahu A, Kurian JS, Tiwari V (2020) Vibronic resonance is inadequately described by one-particle basis sets. J Chem Phys 153(22):224114. https://doi.org/10.1063/5.0029027
Salem L (1979) The sudden polarization effect and its possible role in vision. Acc Chem Res 12(3):87–92. https://doi.org/10.1021/ar50135a002
Sato Y, Navarro Hernández A, Gillespie LD et al (2020) Effects of intramolecular vibrations on excitation energy transfer dynamics of the Fenna-Matthews-Olson complex. Chem Phys 539:110940. https://doi.org/10.1016/j.chemphys.2020.110940
Sauer K (1975) Primary events and the trapping of energy. In: Govindjee (ed) Bioenerg Photosynth, vol 1. Academic Press, New York, pp 115–181
Sauer K (1965) Optical rotatory dispersion of chlorophyll in solution and in chloroplast subunits. Proc Natl Acad Sci USA 53(4):716–722. https://doi.org/10.1073/pnas.53.4.716
Sauer K, Scheer H (1988) Excitation transfer in C-phycocyanin. Forster transfer rate and exciton calculations based on new crystal structure data for C-phycocyanins from Agmenellum quadruplicatum and Mastigocladus laminosus. Biochim Biophys Acta 936:157–170. https://doi.org/10.1016/0005-2728(88)90232-0
Sauer K, Smith JRL, Schultz AJ (1966) The dimerization of chlorophyll a, chlorophyll b, and bacteriochlorophyll in solution. J Am Chem Soc 88(12):2681–2688
Sauer K, Dratz EA, Coyne L (1968) Circular dichroism spectra and the molecular arrangement of bacteriochlorophylls in the reaction centers of photosynthetic bacteria. Proc Natl Acad Sci USA 61(1):17–24. https://doi.org/10.1073/pnas.61.1.17
Scholes GD, Smyth C (2014) Perspective: detecting and measuring exciton delocalization in photosynthetic light harvesting. J Chem Phys 140(11):110901. https://doi.org/10.1063/1.4869329
Scholes GD, Fleming GR, Olaya-Castro A et al (2011) Lessons from nature about solar light harvesting. Nat Chem 3(10):763–774. https://doi.org/10.1038/nchem.1145
Scholes GD, Fleming GR, Chen LX et al (2017) Using coherence to enhance function in chemical and biophysical systems. Nature 543(7647):647–656. https://doi.org/10.1038/nature21425
Siebrand W (1964) Vibrational structure of electronic states of molecular aggregates. I. A variation approach to dimeric systems. J Chem Phys 40(8):2223–2230
Sil S, Tilluck RW, Mohan TMN et al (2022) Excitation energy transfer and vibronic coherence in intact phycobilisomes. Nat Chem 14(11):1286–1294. https://doi.org/10.1038/s41557-022-01026-8
Simpson WT, Peterson DL (1957) Coupling strength for resonance force transfer of electronic energy in van der Waals solids. J Chem Phys 26(3):588–593. https://doi.org/10.1063/1.1743351
Sohoni S, Lloyd LT, Hitchcock A et al (2023) Phycobilisome’s exciton transfer efficiency relies on an energetic funnel driven by chromophore-linker protein interactions. J Am Chem Soc 145(21):11659–11668. https://doi.org/10.1021/jacs.3c01799
Spano FC (2010) The spectral signatures of Frenkel polarons in H- and J-aggregates. Acc Chem Res 43(3):429–439. https://doi.org/10.1021/ar900233v
Tang K, Ding WL, Höppner A et al (2015) The terminal phycobilisome emitter, LCM: a light-harvesting pigment with a phytochrome chromophore. Proc Natl Acad Sci USA 112(52):15880–15885. https://doi.org/10.1073/pnas.1519177113
Tanimura Y, Kubo R (1989) Time evolution of a quantum system in contact with a nearly Gaussian-Markoffian noise bath. J Phys Soc Jpn 58(1):101–114. https://doi.org/10.1143/JPSJ.58.101
Tavan P, Schulten K (1987) Electronic excitations in finite and infinite polyenes. Phys Rev B Condens Matter 36(8):4337–4358. https://doi.org/10.1103/PhysRevB.36.4337
Thyrhaug E, Tempelaar R, Alcocer MJP et al (2018) Identification and characterization of diverse coherences in the Fenna-Matthews-Olson complex. Nat Chem 10(7):780–786. https://doi.org/10.1038/s41557-018-0060-5
Tian L, van Stokkum IHM, Koehorst RBM et al (2011) Site, rate, and mechanism of photoprotective quenching in cyanobacteria. J Am Chem Soc 133(45):18304–18311. https://doi.org/10.1021/ja206414m
Tian L, Gwizdala M, van Stokkum IHM et al (2012) Picosecond kinetics of light harvesting and photoprotective quenching in wild-type and mutant phycobilisomes isolated from the cyanobacterium Synechocystis PCC 6803. Biophys J 102(7):1692–1700. https://doi.org/10.1016/j.bpj.2012.03.008
Tilluck RW, Ghosh S, Guberman-Pfeffer MJ et al (2021) Interexciton nonradiative relaxation pathways in the peridinin-chlorophyll protein. Cell Reports Phys Sci 2(3):100380. https://doi.org/10.1016/j.xcrp.2021.100380
Tilluck RW, Mohan TMN, Hetherington CV et al (2021) Vibronic excitons and conical intersections in semiconductor quantum dots. J Phys Chem Lett 12:9677–9683. https://doi.org/10.1021/acs.jpclett.1c02630
Tiwari V, Jonas DM (2018) Electronic energy transfer through non-adiabatic vibrational-electronic resonance. II. 1D spectra for a dimer. J Chem Phys 148(8):084308. https://doi.org/10.1063/1.5003193
Tiwari V, Peters WK, Jonas DM (2013) Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework. Proc Natl Acad Sci USA 110(4):1203–1208. https://doi.org/10.1073/pnas.1211157110
Tiwari V, Peters WK, Jonas DM (2017) Electronic energy transfer through non-adiabatic vibrational-electronic resonance. I. Theory for a dimer. J Chem Phys 147(15):154308. https://doi.org/10.1063/1.5005835
Tronrud DE, Wen J, Gay L et al (2009) The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria. Photosynth Res 100:79–87. https://doi.org/10.1007/s11120-009-9430-6
Vermeglio A, Paillotin G (1982) Structure of Rhodopseudomonas viridis reaction centers. Absorption and photoselection at low temperature. Biochim Biophys Acta Bioenerg 681(1):32–40. https://doi.org/10.1016/0005-2728(82)90275-4
Vulto SIE, Neerken S, Louwe RJW et al (1998) Excited-state structure and dynamics in FMO antenna complexes from photosynthetic green sulfur bacteria. J Phys Chem B 102(51):10630–10635. https://doi.org/10.1021/jp983003v
Wahadoszamen M, Krüger TPJ, Ara AM et al (2020) Charge transfer states in phycobilisomes. Biochim Biophys Acta Bioenerg 7:148187. https://doi.org/10.1016/j.bbabio.2020.148187
Wahadoszamen M, Margalit I, Ara AM et al (2014) The role of charge-transfer states in energy transfer and dissipation within natural and artificial bacteriochlorophyll proteins. Nat Commun 5:5287. https://doi.org/10.1038/ncomms6287
Warshel A (1976) Bicycle-pedal model for the first step in the vision process. Nature 260(5553):679–683. https://doi.org/10.1038/260679a0
Warshel A (1980) Role of the chlorophyll dimer in bacterial photosynthesis. Proc Natl Acad Sci USA 77(6):3105–3109. https://doi.org/10.1073/pnas.77.6.3105
Warshel A, Parson WW (1987) Spectroscopic properties of photosynthetic reaction centers. 1. Theory. J Am Chem Soc 109(20):6143–6152. https://doi.org/10.1021/ja00254a039
Womick JM, Moran AM (2009) Exciton coherence and energy transport in the light-harvesting dimers of allophycocyanin. J Phys Chem B 113(48):15747–15759. https://doi.org/10.1021/jp907644h
Womick JM, Moran AM (2009) Nature of excited states and relaxation mechanisms in C-phycocyanin. J Phys Chem B 113(48):15771–15782. https://doi.org/10.1021/jp908093x
Womick JM, Moran AM (2011) Vibronic enhancement of exciton sizes and energy transport in photosynthetic complexes. J Phys Chem B 115(6):1347–1356. https://doi.org/10.1021/jp106713q
Womick JM, Liu H, Moran AM (2011) Exciton delocalization and energy transport mechanisms in R-phycoerythrin. J Phys Chem A 115(12):2471–2482. https://doi.org/10.1021/jp111720a
Won Y, Friesner RA (1988) Simulation of optical spectra from the reaction center of Rhodopseudomonas viridis. J Phys Chem 92:2208–2014. https://doi.org/10.1021/j100319a025
Yang M, Fleming GR (2002) Influence of phonons on exciton transfer dynamics: comparison of the Redfield, Forster, and modified Redfield equations. Chem Phys 282(1):163–180. https://doi.org/10.1016/S0301-0104(02)00604-3
Yarkony DR (2001) Conical intersections: the new conventional wisdom. J Phys Chem A 105(26):6277–6293. https://doi.org/10.1021/jp003731u
Yarkony DR (2012) Nonadiabatic quantum chemistry-past, present, and future. Chem Rev 112(1):481–498. https://doi.org/10.1021/cr2001299
Zhang WM, Meier T, Chernyak V et al (1998) Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J Chem Phys 108(18):7763–7774. https://doi.org/10.1063/1.476212
Acknowledgements
This article is dedicated to the memory of Professor Kenneth Sauer, who served as the author’s postdoctoral research advisor during his Miller Fellowship at the University of California, Berkeley. The author was aided by several discussions with Professor Benjamin Levine (Stony Brook University).
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Work in the laboratory of W.F.B. was supported by grant award DE-SC0010847 from the Photosynthetic Systems program of the Office of Basic Energy Sciences, U.S. Department of Energy.
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Beck, W.F. Intramolecular charge transfer and the function of vibronic excitons in photosynthetic light harvesting. Photosynth Res (2024). https://doi.org/10.1007/s11120-024-01095-5
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DOI: https://doi.org/10.1007/s11120-024-01095-5