Coherent phenomena in photosynthetic light harvesting: part two—observations in biological systems

Abstract

Considerable debate surrounds the question of whether or not quantum mechanics plays a significant, non-trivial role in photosynthetic light harvesting. Many have proposed that quantum superpositions and/or quantum transport phenomena may be responsible for the efficiency and robustness of energy transport present in biological systems. The critical experimental observations comprise the observation of coherent oscillations or Bquantum beats^via femtosecond laser spectroscopy, which have been observed in many different light harvesting systems. Part Two of this review aims to provide an overview of experimental observations of energy transfer in the most studied light harvesting systems. Length scales, derived from crystallographic studies, are combined with energy and time scales of the beats observed via spectroscopy. A consensus is emerging that most long-lived (hundreds of femtoseconds) coherent phenomena are of vibrational or vibronic origin, where the latter may result in coherent excitation transport within a protein complex. In contrast, energy transport between proteins is likely to be incoherent in nature. The question of whether evolution has selected for these non-trivial quantum phenomena may be an unanswerable question, as dense packings of chromophores will lead to strong coupling and hence non-trivial quantum phenomena. As such, one cannot discern whether evolution has optimised light harvesting systems for high chromophore density or for the ensuing quantum effects as these are inextricably linked and cannot be switched off.

Energy transfer dynamics in B-phycoerythrin from the red alga Porphyridium purpureum

“…The results show that three pairs of exciton-coupled chromophore pairs can be formed in PE545 and PC645, two of which are in the monomer and one pair on the surface between the monomers [16,17]. In recent years, based on two-dimensional photon echo spectroscopy, the results show that the energy transfer of the internal chromophores of cryptophyte phycobiliproteins may be in a network state linked by quantum correlation [18][19][20][21][22][23]. However, in red algae and cyanobacteria, it is unclear whether exciton coupling mechanism exists.…”

Do photosynthetic complexes use quantum coherence to increase their efficiency? Probably not

“…The extraction rate can be estimated by considering the time scales of different transport processes that take place in the photosynthetic complexes. For instance, the exciton transfer time between adjacent LH2 complexes was found to be 3 to 100 ps ( 3 , 11 , 14 , 18 , 44 , 52 , 57 ), and the trapping time of energy by the core complexes in PC-645 was found to be ≈100 ps ( 58 ). We then set the extraction rate to an average of γ ext = 0.1 ps −1 .…”

“…Interest in the dynamics of excitons in the ETC exploded over the past decade, following recent experiments, where ultrafast nonlinear spectroscopy signals showed long-lived oscillations (2)(3)(4)(5)(6)(7)(8). The discovery of coherent oscillations in ETCs pushed forward the hypothesis that in natural photosynthetic complexes, which are extremely efficient, quantum coherence in the presence of an environment is used to assist energy transfer, an idea that has generated much excitement (and debate) (9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19).…”

Scaffolding proteins guide the evolution of algal light harvesting antennas

“…Light harvesting antennas of photosynthetic organisms are incredibly diverse 1 – 3 and the history of algal endosymbioses presents a challenge in determining their origins 4 – 8 . Most extant photosynthetic eukaryotes resulted from a single primary endosymbiosis where a cyanobacterium became the ancestral chloroplast.…”