Quantum Coherent Excitation Energy Transfer by Carotenoids in Photosynthetic Light Harvesting

Abstract

It remains an open question whether quantum coherence and molecular excitons created by delocalization of electronic excited states are essential features of the mechanisms that enable efficient light capture and excitation energy transfer to reaction centers in photosynthetic organisms. The peridinin-chlorophyll a protein from marine dinoflagellates is an example of a light-harvesting system with tightly clustered antenna chromophores in which quantum coherence has long been suspected, but unusually it features the carotenoid peridinin as the principal light absorber for mid-visible photons. We report that broad-band two-dimensional electronic spectroscopy indeed reveals the initial presence of exciton relaxation pathways that enable transfer of excitation from peridinin to chlorophyll a in <20 fs, but the quantum coherence that permits this is very short-lived. Strongly coupled excited-state vibrational distortions of the peridinins trigger a dynamic transition of the electronic structure of the system and a rapid conversion to incoherent energy transfer mechanisms.

Room temperature quantum coherence vs. electron transfer in a rhodanine derivative chromophore

“…The studied D2F complex exhibits a long-term coherence that is comparable to the ones experimentally found in some light-harvesting and organic materials 3,4,[16][17][18] . As shown in Fig.…”

“…From a perspective of novel materials and technologies for solar energy conversion, organic photovoltaic (OPV) sytems have attracted significant attention [7][8][9] due to the enhancement of their power conversion efficiency (PCE) 5,6 , flexibility,manufacturing reduction costs, and high-temperature production of cells [10][11][12][13][14] . On a different facet, but complementary to this development, quantum coherence has, over the past decade, been experimentally linked to early-stage energy transfer in light harvesting photosynthetic complexes [1][2][3][4][15][16][17][18][19] ; in particular, time-resolved ultrafast optical and electronic spectroscopies have evidenced oscillations of exciton state populations lasting up to a few hundred femtoseconds, which have been attributed to quantum coherence emerging as a result of initially prepared laser pulses [1][2][3][4][15][16][17][18] . This two-way breakthrough poses an intriguing question about the possible functional role of quantum coherent effects as a precursor of efficient ET in materials and biological systems under structural and energetic disorder at physiological conditions.…”

Coherence in carotenoid-to-chlorophyll energy transfer

“…Recently, another kinetic scheme has been proposed to describe EET from S 2 to Q y , which relies on a preliminary step of relaxation of the S 2 state geometry from the Franck-Condon to a distorted conformation 24 . Our quantum chemical calculations, however, seem to rule out the presence of such a preliminary step as there is no trace of relaxed twisted configurations of Per in the S 2 state.…”

“…Like for other antenna complexes bearing Cars, femtosecond spectroscopic experiments on PCP have also suggested the presence of ultrafast channels of EET from S 2 to the Q bands of Chl 4 , 7 – 9 , 23 (Q x and/or vibronic states of Q y ), also with possible contributions of coherent pathways 24 , 25 . However, clear and direct evidence is still lacking to identify the main pathways of energy flow from Pers to Chls, and their timescales, including the role of vibrational modes on the dynamics.…”

Carotenoid-Chlorophyll Interactions in a Photosynthetic Antenna Protein: A Supramolecular QM/MM Approach

“…Recent theoretical [ 14 , 15 ] and experimental [ 15 , 16 , 17 ] work has identified an ultrafast quantum coherent mechanism in the Per-to-Chl a energy transduction process. While it is now well established that Per-to-Chl a energy transfer represents a fundamental event in light harvesting by PCP, it is still unknown if energy transfer paths among Pers, and from multiple Pers to Chl a , help funnel the transfer of energy.…”