Abstract
The role of non-trivial quantum mechanical effects in biology, and especially photosynthesis, has been the subject of intense hype and scrutiny over the past decade. This is largely the product of an increase in temporal, spatial and energetic resolution afforded by modern crystallography and the advent of ultrafast laser spectroscopy. The latter technique has been able to resolve quantum coherent oscillations in the spectroscopic signals of light harvesting proteins, dubbed “quantum beats”, that persist for hundreds of femtoseconds (in the longest-lived cases). Quantum beats are symptomatic of general coherent phenomena and are thus indicative of non-trivial quantum coherent effects in photosynthetic systems. A brief introduction to quantum mechanics is given and the various coherence effects it produces are discussed in detail. Time, length and energy scales of light harvesting systems are presented, providing a context for understanding the possible extent of coherent effects ultimately leading to an understanding of quantum coherent energy transport and the proposal that quantum coherence may be responsible for the efficiency and robustness of energy transport in biological systems, especially in some algae. A consensus is emerging that most long-lived coherent phenomena are of vibrational or vibronic origin, where the latter may result in coherent excitation transport within an algal protein complex, however, it is unlikely that coherent behaviour is present between complexes. Broadly speaking, whether evolution has selected for these non-trivial quantum phenomena may be an unanswerable question as quantum processes come to prominence at the scales of interest for photosynthesis and quantum mechanics that cannot merely be switched on or off.
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References
Adolphs J, Renger T (2006) How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria. Biophys J 91:2778–2797
Allen JF, Martin W (2007) Evolutionary biology: out of thin air. Nature 445:610–612
Arpin PC, Turner DB, McClure SD et al (2015) Spectroscopic studies of cryptophyte light harvesting proteins: vibrations and coherent oscillations. J Phys Chem B 119:10025–10034
Ballottari M, Mozzo M, Girardon J et al (2013) Chlorophyll triplet quenching and photoprotection in the higher plant monomeric antenna protein Lhcb5. J Phys Chem B 117:11337–11348
Berera R, van Grondelle R, Kennis JTM (2009) Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems. Photosynth Res 101:105–118
Bodył A, Moszczyński K (2006) Did the peridinin plastid evolve through tertiary endosymbiosis? A hypothesis. Eur J Phycol 41:435–448
Book LD, Ostafin AE, Ponomarenko N et al (2000) Exciton delocalization and initial dephasing dynamics of purple bacterial LH2. J Phys Chem B 104:8295–8307
Bricker W, Lo C (2015) Efficient pathways of excitation energy transfer from delocalized excitons in the peridinin–chlorophyll –protein complex. J Phys Chem B 119(18):5755–5764
Cardona T (2014) A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth Res 126:111–134
Chachisvilis M, Sundström V (1996) Femtosecond vibrational dynamics and relaxation in the core light-harvesting complex of photosynthetic purple bacteria. Chem Phys Lett 261:165–174
Chachisvilis M, Kühn O, Pullerits T, Sundström V (1997) Excitons in photosynthetic purple bacteria: wavelike motion or incoherent hopping? J Phys Chem B 101:7275–7283
Cheng Y-C, Fleming GR (2008) Coherence quantum beats in two-dimensional electronic spectroscopy. J Phys Chem A 112:4254–4260
Chmeliov J, Songaila E, Rancova O et al (2013) Excitons in the LH3 complexes from purple bacteria. J Phys Chem B 117:11058–11068
Christensson N, Kauffmann HF, Pullerits T, Mančal T (2012) Origin of long-lived coherences in light-harvesting complexes. J Phys Chem B 116:7449–7454
Cohen Stuart TA, Vengris M, Novoderezhkin VI et al (2011) Direct visualization of exciton reequilibration in the LH1 and LH2 complexes of Rhodobacter sphaeroides by multipulse spectroscopy. Biophys J 100:2226–2233
Collini E (2012) Differences among coherent dynamics in evolutionary related light-harvesting complexes: evidence for subtle quantum-mechanical strategies for energy transfer optimization. In: Quantum optics II. SPIE, Bellingham
Collini E, Wong CY, Wilk KE et al (2010) Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463:644–647
Curtis BA, Tanifuji G, Burki F et al (2012) Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature 492:59–65
Dahlberg PD, Norris GJ, Wang C et al (2015) Communication: coherences observed in vivo in photosynthetic bacteria using two-dimensional electronic spectroscopy. J Chem Phys 143:101101
Dean JC, Mirkovic T, Toa ZSD et al (2016) Vibronic enhancement of algae light harvesting. Chem 1:858–872
Delaye L, Valadez-Cano C, Pérez-Zamorano B (2016) How really ancient is Paulinella Chromatophora? PLoS Curr 8. https://doi.org/10.1371/currents.tol.e68a099364bb1a1e129a17b4e06b0c6b
Di Valentin M, Carbonera D (2017) The fine tuning of carotenoid–chlorophyll interactions in light-harvesting complexes: an important requisite to guarantee efficient photoprotection via triplet–triplet energy transfer in the complex balance of the energy transfer processes. J Phys B Atomic Mol Phys 50:162001
Diffey WM, Homoelle BJ, Edington MD, Beck WF (1998) Excited-state vibrational coherence and anisotropy decay in the Bacteriochlorophyll a Dimer protein B820. J Phys Chem B 102:2776–2786
Dostál J, Mančal T, Vácha F et al (2014) Unraveling the nature of coherent beatings in chlorosomes. J Chem Phys 140:115103
Dostál J, Pšenčík J, Zigmantas D (2016) In situ mapping of the energy flow through the entire photosynthetic apparatus. Nat Chem 8:705–710
Doust AB, Marai CNJ, Harrop SJ et al (2004) Developing a structure–function model for the Cryptophyte Phycoerythrin 545 using ultrahigh resolution crystallography and ultrafast laser spectroscopy. J Mol Biol 344:135–153
Duan H-G, Stevens AL, Nalbach P et al (2015) Two-dimensional electronic spectroscopy of light-harvesting complex II at ambient temperature: a joint experimental and theoretical study. J Phys Chem B 119:12017–12027
Duan H-G, 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 114:8493–8498
Edington MD, Riter RE, Beck WF (1995) Evidence for coherent energy transfer in Allophycocyanin Trimers. J Phys Chem 99:15699–15704
Engel GS, Calhoun TR, Read EL et al (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782–786
Ferretti M, Novoderezhkin VI, Romero E et al (2014) The nature of coherences in the B820 bacteriochlorophyll dimer revealed by two-dimensional electronic spectroscopy. Phys Chem Chem Phys 16:9930–9939
Fidler AF, Harel E, Engel GS (2010) Dissecting hidden couplings using fifth-order three-dimensional electronic spectroscopy. J Phys Chem Lett 1:2876–2880
Fidler AF, Singh VP, Long PD et al (2013) Time scales of coherent dynamics in the light-harvesting complex 2 (LH2) of Rhodobacter sphaeroides. J Phys Chem Lett 4:1404–1409
Fujimoto KJ, Balashov SP (2017) Vibronic coupling effect on circular dichroism spectrum: carotenoid–retinal interaction in xanthorhodopsin. J Chem Phys 146:095101
Fuller FD, Pan J, Gelzinis A et al (2014) Vibronic coherence in oxygenic photosynthesis. Nat Chem 6:706–711
Gantt E (1971) Chloroplast structure of the cryptophyceae: evidence for phycobiliproteins within intrathylakoidal spaces. J Cell Biol 48:280–290
Goodknight J, Aspuru-Guzik A (2017) Taking six-dimensional spectra in finite time. Science 356:1333
Gould SB, Fan E, Hempel F et al (2007) Translocation of a phycoerythrin α subunit across five biological membranes. J Biol Chem 282:30295–30302
Green BR (2011) Chloroplast genomes of photosynthetic eukaryotes. Plant J 66:34–44
Harel E (2018) Zooming in on vibronic structure by lowest-value projection reconstructed 4D coherent spectroscopy. J Chem Phys 148:194201
Harel E, Engel GS (2012) Quantum coherence spectroscopy reveals complex dynamics in bacterial light-harvesting complex 2 (LH2). Proc Natl Acad Sci U S A 109:706–711
Harrop SJ, Wilk KE, Dinshaw R et al (2014) Single-residue insertion switches the quaternary structure and exciton states of cryptophyte light-harvesting proteins. Proc Natl Acad Sci U S A 111:E2666–E2675
Hayes D, Panitchayangkoon G, Fransted KA et al (2010) Dynamics of electronic dephasing in the Fenna–Matthews–Olson complex. New J Phys 12:065042
Hayes D, Wen J, Panitchayangkoon G et al (2011) Robustness of electronic coherence in the Fenna–Matthews–Olson complex to vibronic and structural modifications. Faraday Discuss 150:459
Hildner R, Brinks D, Nieder JB et al (2013) Quantum coherent energy transfer over varying pathways in single light-harvesting complexes. Science 340:1448–1451
Hofmann E, Wrench PM, Sharples FP et al (1996) Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science 272:1788–1791
Hutson WO, Spencer AP, Harel E (2018) Ultrafast four-dimensional coherent spectroscopy by projection reconstruction. J Phys Chem Lett 9:1034–1040
Jonas DM (2003) Two-dimensional femtosecond spectroscopy. Annu Rev Phys Chem 54:425–463
Jumper CC, Rafiq S, Wang S, Scholes GD (2018a) From coherent to vibronic light harvesting in photosynthesis. Curr Opin Chem Biol 47:39–46
Jumper CC, van Stokkum IHM, Mirkovic T, Scholes GD (2018b) Vibronic wavepackets and energy transfer in cryptophyte light-harvesting complexes. J Phys Chem B 122:6328–6340
Jun S, Yang C, Isaji M et al (2014) Coherent oscillations in chlorosome elucidated by two-dimensional electronic spectroscopy. J Phys Chem Lett 5:1386–1392
Kim H, Li H, Maresca JA et al (2007) Triplet exciton formation as a novel photoprotection mechanism in chlorosomes of Chlorobium tepidum. Biophys J 93:192–201
Kraack JP, Buckup T, Hampp N, Motzkus M (2011) Ground- and excited-state vibrational coherence dynamics in Bacteriorhodopsin probed with degenerate four-wave-mixing experiments. ChemPhysChem 12:1851–1859
Lee H, Cheng Y-C, Fleming GR (2007) Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science 316:1462–1465
Lewis NHC, Gruenke NL, Oliver TAA et al (2016) Observation of electronic excitation transfer through light harvesting complex II using two-dimensional electronic-vibrational spectroscopy. J Phys Chem Lett. https://doi.org/10.1021/acs.jpclett.6b02280
Loukianov A, Niedringhaus A, Berg B et al (2017) Two-dimensional electronic stark spectroscopy. J Phys Chem Lett 8:679–683
Ma Y-Z, Aschenbrücker J, Miller M, Gillbro T (1999) Ground-state vibrational coherence in chlorosomes of the green sulfur photosynthetic bacterium Chlorobium phaeobacteroides. Chem Phys Lett 300:465–472
Ma F, Yu L-J, Hendrikx R et al (2017) Excitonic and vibrational coherence in the excitation relaxation process of two LH1 complexes as revealed by two-dimensional electronic spectroscopy. J Phys Chem Lett 8:2751–2756
Ma F, Romero E, Jones MR et al (2018) Vibronic coherence in the charge separation process of the Rhodobacter sphaeroides reaction center. J Phys Chem Lett 9:1827–1832
MacColl R, Eisele LE, Marrone J (1999) Fluorescence polarization studies on four biliproteins and a Bilin model for phycoerythrin 545. Biochim Biophys Acta Bioenerg 1412:230–239
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 10:177–183
Marin A, Doust AB, Scholes GD et al (2011) Flow of excitation energy in the cryptophyte light-harvesting antenna phycocyanin 645. Biophys J 101:1004–1013
McClure SD, Turner DB, Arpin PC et al (2014) Coherent oscillations in the PC577 Cryptophyte antenna occur in the excited electronic state. J Phys Chem B 118:1296–1308
Mirkovic T, Ostroumov EE, Anna JM et al (2016) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117:249–293
Morden CW, Sherwood AR (2002) Continued evolutionary surprises among dinoflagellates. Proc Natl Acad Sci U S A 99:11558–11560
Müh F, Renger T (2012) Refined structure-based simulation of plant light-harvesting complex II: linear optical spectra of trimers and aggregates. Biochim Biophys Acta 1817:1446–1460
Nango E, Royant A, Kubo M et al (2016) A three-dimensional movie of structural changes in bacteriorhodopsin. Science 354:1552–1557
Neilson JAD, Durnford DG (2010) Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth Res 106:57–71
Nogly P, Weinert T, James D et al (2018) Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser. Science 361. https://doi.org/10.1126/science.aat0094
Novelli F, Nazir A, Richards GH et al (2015) Vibronic resonances facilitate excited-state coherence in light-harvesting proteins at room temperature. J Phys Chem Lett 6:4573–4580
Oesterhelt D, Stoeckenius W (1973) Functions of a new photoreceptor membrane. Proc Natl Acad Sci 70:2853–2857
Oliver TAA, Lewis NHC, Fleming GR (2014) Correlating the motion of electrons and nuclei with two-dimensional electronic-vibrational spectroscopy. Proc Natl Acad Sci U S A 111:10061–10066
Paleček D, Edlund P, Westenhoff S, Zigmantas D (2017) Quantum coherence as a witness of vibronically hot energy transfer in bacterial reaction center. Sci Adv 3:e1603141
Panitchayangkoon G, Hayes D, Fransted KA et al (2010) Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc Natl Acad Sci U S A 107:12766–12770
Panitchayangkoon G, Voronine DV, Abramavicius D et al (2011) Direct evidence of quantum transport in photosynthetic light-harvesting complexes. Proc Natl Acad Sci U S A 108:20908–20912
Prokhorenko VI, Steensgaard DB, Holzwarth AR (2000) Exciton dynamics in the chlorosomal antennae of the green bacteria Chloroflexus aurantiacus and Chlorobium tepidum. Biophys J 79:2105–2120
Prokhorenko VI, Nagy AM, Waschuk SA et al (2006) Coherent control of retinal isomerization in bacteriorhodopsin. Science 313:1257–1261
Ramanan C, Ferretti M, van Roon H et al (2017) Evidence for coherent mixing of excited and charge-transfer states in the major plant light-harvesting antenna, LHCII. Phys Chem Chem Phys 19:22877–22886
Raszewski G, Diner BA, Schlodder E, Renger T (2008) Spectroscopic properties of reaction center pigments in photosystem II core complexes: revision of the multimer model. Biophys J 95:105–119
Rathbone H, Davis J, Michie K, Goodchild S, Robertson N, Curmi P (2018a) Coherent phenomena in photosynthetic light harvesting: part one–theory and spectroscopy. Biophys Rev 10:1427–1441
Rathbone H, Davis J, Michie K, Goodchild S, Robertson N, Curmi P (2018b) Coherent phenomena in photosynthetic light harvesting: part two–observations in biological systems. Biophys Rev 10(5):1443–1463
Raymond J, Zhaxybayeva O, Gogarten JP et al (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298:1616–1620
Rebentrost P, Mohseni M, Kassal I et al (2009) Environment-assisted quantum transport. New J Phys 11:033003
Richards GH, Wilk KE, Curmi PMG, Davis JA (2014) Disentangling electronic and vibrational coherence in the Phycocyanin-645 light-harvesting complex. J Phys Chem Lett 5:43–49
Roach T, Krieger-Liszkay A (2012) The role of the PsbS protein in the protection of photosystems I and II against high light in Arabidopsis thaliana. Biochim Biophys Acta 1817:2158–2165
Rolczynski BS, Zheng H, Singh VP et al (2018) Correlated protein environments drive quantum coherence lifetimes in photosynthetic pigment-protein complexes. Chem 4:138–149
Romero E, Augulis R, Novoderezhkin VI et al (2014) Quantum coherence in photosynthesis for efficient solar-energy conversion. Nat Phys 10:676–682
Romero E, Prior J, Chin AW et al (2017) Quantum – coherent dynamics in photosynthetic charge separation revealed by wavelet analysis. Sci Rep 7. https://doi.org/10.1038/s41598-017-02906-7
Roscioli JD, Ghosh S, LaFountain AM et al (2017) Quantum coherent excitation energy transfer by carotenoids in photosynthetic light harvesting. J Phys Chem Lett 8:5141–5147
Sarkisov OM, Gostev FE, Shelaev IV et al (2006) Long-lived coherent oscillations of the femtosecond transients in cyanobacterial photosystem I. Phys Chem Chem Phys 8:5671–5678
Savikhin S, Zhu Y, Lin S et al (1994) Femtosecond spectroscopy of Chlorosome antennas from the Green photosynthetic bacterium Chloroflexus aurantiacus. J Phys Chem 98:10322–10334
Savikhin S, van Noort PI, Blankenship RE, Struve WS (1995a) Femtosecond probe of structural analogies between chlorosomes and bacteriochlorophyll c aggregates. Biophys J 69:1100–1104
Savikhin S, van Noort PI, Zhu Y et al (1995b) Ultrafast energy transfer in light-harvesting chlorosomes from the green sulfur bacterium Chlorobium tepidum. Chem Phys 194:245–258
Schlau-Cohen GS, Ishizaki A, Calhoun TR et al (2012) Elucidation of the timescales and origins of quantum electronic coherence in LHCII. Nat Chem 4:389–395
Scholes GD, Mirkovic T, Turner DB et al (2012) Solar light harvesting by energy transfer: from ecology to coherence. Energy Environ Sci 5:9374
Singh VP, Westberg M, Wang C et al (2015) Towards quantification of vibronic coupling in photosynthetic antenna complexes. J Chem Phys 142:212446
Spörlein S, Zinth W, Wachtveitl J (1998) Vibrational coherence in photosynthetic reaction centers observed in the Bacteriochlorophyll anion band. J Phys Chem B 102:7492–7496
Streltsov AM, Vulto SIE Y, Shkuropatov A et al (1998) BAand BBAbsorbance perturbations induced by coherent nuclear motions in reaction centers from Rhodobacter sphaeroidesupon 30-fs excitation of the primary donor. J Phys Chem B 102:7293–7298
Strümpfer J, Schulten K (2009) Light harvesting complex II B850 excitation dynamics. J Chem Phys 131:225101
Thyrhaug E, Žídek K, Dostál J et al (2016) Exciton structure and energy transfer in the Fenna–Matthews–Olson complex. J Phys Chem Lett 7:1653–1660
Thyrhaug E, Tempelaar R, Alcocer MJP et al (2018) Identification and characterization of diverse coherences in the Fenna–Matthews–Olson complex. Nat Chem. https://doi.org/10.1038/s41557-018-0060-5
Turner DB, Wilk KE, Curmi PMG, Scholes GD (2011) Comparison of electronic and vibrational coherence measured by two-dimensional electronic spectroscopy. J Phys Chem Lett 2:1904–1911
Turner DB, Dinshaw R, Lee K-K et al (2012) Quantitative investigations of quantum coherence for a light-harvesting protein at conditions simulating photosynthesis. Phys Chem Chem Phys 14:4857–4874
van der Weij-De Wit CD, Doust AB, van Stokkum IHM et al (2006) How energy funnels from the phycoerythrin antenna complex to photosystem I and photosystem II in cryptophyte Rhodomonas CS24 cells. J Phys Chem B 110:25066–25073
Vos MH, Lambry JC, Robles SJ et al (1991) Direct observation of vibrational coherence in bacterial reaction centers using femtosecond absorption spectroscopy. Proc Natl Acad Sci U S A 88:8885–8889
Vos MH, Jones MR, Hunter CN et al (1994) Coherent dynamics during the primary electron-transfer reaction in membrane-bound reaction centers of Rhodobacter sphaeroides. Biochemistry 33:6750–6757
Vos MH, Jones MR, Martin J-L (1998) Vibrational coherence in bacterial reaction centers: spectroscopic characterisation of motions active during primary electron transfer. Chem Phys 233:179–190
Wells KL, Lambrev PH, Zhang Z et al (2014) Pathways of energy transfer in LHCII revealed by room-temperature 2D electronic spectroscopy. Phys Chem Chem Phys 16:11640–11646
Westenhoff S, Paleček D, Edlund P et al (2012) Coherent picosecond Exciton dynamics in a photosynthetic reaction center. J Am Chem Soc 134:16484–16487
Wilk KE, Harrop SJ, Jankova L et al (1999) Evolution of a light-harvesting protein by addition of new subunits and rearrangement of conserved elements: crystal structure of a cryptophyte phycoerythrin at 1.63-a resolution. Proc Natl Acad Sci U S A 96:8901–8906
Womick JM, Moran AM (2009) Exciton coherence and energy transport in the light-harvesting dimers of allophycocyanin. J Phys Chem B 113:15747–15759
Wong CY, Alvey RM, Turner DB et al (2012) Electronic coherence lineshapes reveal hidden excitonic correlations in photosynthetic light harvesting. Nat Chem 4:396–404
Yin Y, Katsanos DE, Evangelou SN (2008) Quantum walks on a random environment. Phys Rev A 77. https://doi.org/10.1103/physreva.77.022302
Young HT, Edwards SA, Gräter F (2013) How fast does a signal propagate through proteins? PLoS One 8:e64746
Zhang JM, Shiu YJ, Hayashi M et al (2001) Investigations of ultrafast Exciton dynamics in Allophycocyanin Trimer†. J Phys Chem A 105:8878–8891
Zhang Z, Wells KL, Seidel MT, Tan H-S (2013) Fifth-order three-dimensional electronic spectroscopy using a pump-probe configuration. J Phys Chem B 117:15369–15385
Zhang J, Ma J, Liu D et al (2017) Structure of phycobilisome from the red alga Griffithsia pacifica. Nature 551:57–63
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Rathbone, H.W., Davis, J.A., Curmi, P.M.G. (2020). Coherent Processes in Photosynthetic Energy Transport and Transduction. In: Larkum, A., Grossman, A., Raven, J. (eds) Photosynthesis in Algae: Biochemical and Physiological Mechanisms. Advances in Photosynthesis and Respiration, vol 45. Springer, Cham. https://doi.org/10.1007/978-3-030-33397-3_15
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