Quantum coherence in the photosynthesis apparatus of living cyanobacteria (original) (raw)

Long-range quantum coherence of the photosystem 2 complexes in living cyanobacteria

2019

The first step in photosynthesis is an extremely efficient energy transfer mechanism, which is difficult to be explained by classical short-range energy migration (“hopping”) and led to the debate to which extent quantum coherence is involved in the energy transfer between the photosynthetic pigments. Embedding living cyanobacteria between the mirrors of an optical microresonator and using low intensity white light irradiation we observe vacuum Rabi splitting in the transmission and fluorescence spectra as a result of strong light matter coupling of the chlorophyll and the resonator modes. The Rabi-splitting scales with the number of chlorophyll a pigments involved in coherent coupling indicating forming a polaritonic state which is delocalized over the entire cyanobacterial thylakoid system, down to the single photon level. Our data provide evidence that a delocalized polaritonic state is the basis of the extremely high energy transfer efficiency under natural conditions.

Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems

Nature, 2007

Photosynthetic complexes are exquisitely tuned to capture solar light efficiently, and then transmit the excitation energy to reaction centres, where long term energy storage is initiated. The energy transfer mechanism is often described by semiclassical models that invoke 'hopping' of excited-state populations along discrete energy levels 1,2 . Two-dimensional Fourier transform electronic spectroscopy 3-5 has mapped 6 these energy levels and their coupling in the Fenna-Matthews-Olson (FMO) bacteriochlorophyll complex, which is found in green sulphur bacteria and acts as an energy 'wire' connecting a large peripheral light-harvesting antenna, the chlorosome, to the reaction centre 7-9 . The spectroscopic data clearly document the dependence of the dominant energy transport pathways on the spatial properties of the excited-state wavefunctions of the whole bacteriochlorophyll complex 6,10 . But the intricate dynamics of quantum coherence, which has no classical analogue, was largely neglected in the analyses-even though electronic energy transfer involving oscillatory populations of donors and acceptors was first discussed more than 70 years ago 11 , and electronic quantum beats arising from quantum coherence in photosynthetic complexes have been predicted 12,13 and indirectly observed 14 . Here we extend previous twodimensional electronic spectroscopy investigations of the FMO bacteriochlorophyll complex, and obtain direct evidence for remarkably long-lived electronic quantum coherence playing an important part in energy transfer processes within this system. The quantum coherence manifests itself in characteristic, directly observable quantum beating signals among the excitons within the Chlorobium tepidum FMO complex at 77 K. This wavelike characteristic of the energy transfer within the photosynthetic complex can explain its extreme efficiency, in that it allows the complexes to sample vast areas of phase space to find the most efficient path.

Microscopic quantum coherence in a photosynthetic-light-harvesting antenna

2012

Abstract We briefly review the coherent quantum beats observed in recent two-dimensional electronic spectroscopy experiments in a photosynthetic-light-harvesting antenna. We emphasize that the decay of the quantum beats in these experiments is limited by ensemble averaging. The in vivo dynamics of energy transport depends upon the local fluctuations of a single photosynthetic complex during the energy transfer time (a few picoseconds).

Quantum coherence in photosynthetic complexes

2011

The initial steps of photosynthesis require the absorption and subsequent transfer of energy through an intricate network of pigment-protein complexes. Held within the protein scaffold of these complexes, chromophore molecules are densely packed and fixed in specific geometries relative to one another resulting in Coulombic coupling. Excitation energy transfer through these systems can be accomplished with near unity quantum efficiency [Wraight and Clayton, Biochim. Biophys. Acta 333, 246 (1974)]. While replication of this feat is desirable for artificial photosynthesis, the mechanism by which nature achieves this efficiency is unknown. Recent experiments have revealed the presence of long-lived quantum coherences in photosynthetic pigment-protein complexes spanning bacterial and plant species with a variety of functions and compositions. Its ubiquitous presence and wavelike energy transfer implicate quantum coherence as key to the high efficiency achieved by photosynthesis.

Coherence in energy transfer and photosynthesis

Annual review of physical chemistry, 2015

Ultrafast energy transfer is used to transmit electronic excitation among the many molecules in photosynthetic antenna complexes. Recent experiments and theories have highlighted the role of coherent transfer in femtosecond studies of these proteins, suggesting the need for accurate dynamical models to capture the subtle characteristics of energy transfer mechanisms. Here we discuss how to think about coherence in light harvesting and electronic energy transfer. We review the various fundamental concepts of coherence, spanning from classical phenomena to the quantum superposition, and define coherence in electronic energy transfer. We describe the current status of experimental studies on light-harvesting complexes. Insights into the microscopic process are presented to highlight how and why this is a challenging problem to elucidate. We present an overview of the applicable dynamical theories to model energy transfer in the intermediate coupling regime.

Quantum Coherence in Photosynthetic Light Harvesting

2012

Recent two-dimensional (2D) electronic spectroscopic experiments revealed that electronic energy transfer in photosynthetic light harvesting involves long-lived quantum coherence among electronic excitations of pigments. These findings have led to the suggestion that quantum coherence might play a role in achieving the remarkable quantum efficiency of photosynthetic light harvesting.

Electronic coherence effects in photosynthetic light harvesting

Procedia Chemistry, 2011

Photosynthetic light harvesting is a paradigmatic example for quantum effects in biology. In this work, we review studies on quantum coherence effects in the LH2 antenna complex from purple bacteria to demonstrate how quantum mechanical rules play important roles in the speedup of excitation energy transfer, the stabilization of electronic excitations, and the robustness of light harvesting in photosynthesis. Subsequently, we present our recent theoretical studies on exciton dynamical localization and excitonic coherence generation in photosynthetic systems. We apply a variational-polaron approach to investigate decoherence of exciton states induced by dynamical fluctuations due to system-environment interactions. The results indicate that the dynamical localization of photoexcitations in photosynthetic complexes is significant and imperative for a complete understanding of coherence and excitation dynamics in photosynthesis. Moreover, we use a simple model to investigate quantum coherence effects in intercomplex excitation energy transfer in natural photosynthesis, with a focus on the likelihoods of generating excitonic coherences during the process. Our model simulations reveal that excitonic coherence between acceptor exciton states and transient nonlocal quantum correlation between distant pairs of chromophores can be generated through intercomplex energy transfer. Finally, we discuss the implications of these theoretical works and important open questions that remain to be answered.

Quantum biology revisited

Science Advances, 2020

Photosynthesis is a highly optimized process from which valuable lessons can be learned about the operating principles in nature. Its primary steps involve energy transport operating near theoretical quantum limits in efficiency. Recently, extensive research was motivated by the hypothesis that nature used quantum coherences to direct energy transfer. This body of work, a cornerstone for the field of quantum biology, rests on the interpretation of small-amplitude oscillations in two-dimensional electronic spectra of photosynthetic complexes. This Review discusses recent work reexamining these claims and demonstrates that interexciton coherences are too short lived to have any functional significance in photosynthetic energy transfer. Instead, the observed long-lived coherences originate from impulsively excited vibrations, generally observed in femtosecond spectroscopy. These efforts, collectively, lead to a more detailed understanding of the quantum aspects of dissipation. Nature, ...

Realistic Quantum Control of Energy Transfer in Photosynthetic Processes

Energies, 2016

The occurrence of coherence phenomenon as a result of the interference of the probability amplitude terms is among the principle features of quantum mechanics concepts. Current experiments display the presence of quantum techniques whose coherence is supplied over large interval times. Specifically, photosynthetic mechanisms in light-harvesting complexes furnish oscillatory behaviors owing to quantum coherence. In this manuscript, we study the coherent quantum energy transfer for a single-excitation and nonlocal correlation in a dimer system (donor+acceptor) displayed by two-level systems (TLSs), interacting with a cavity field with a time-dependent coupling effect considering the realistic situation of coupling between each TLS and the cavity field. We analyze and explore the specific conditions which are viable with real experimental realization for the ultimate transfer of quantum energy and nonlocal quantum correlation. We show that the enhancement of the probability for a single-excitation energy transfer greatly benefits from the energy detuning, photon-number transition, classicality of the field, and the time-dependent coupling effect. We also find that the entanglement between the donor and acceptor is very sensitive to the physical parameters and it can be generated during the coherent energy transfer.

From coherent to vibronic light harvesting in photosynthesis

Current opinion in chemical biology, 2018

Photosynthetic organisms are a remarkable example of nanoscale engineering and have mastered the process of solar energy harvesting over billions of years of evolution. Therefore, researchers seek insights from the light collection mechanisms of photosynthetic machinery. The initial energy transfer stage of photosynthesis, which begins with light absorption and leads to charge separation, is remarkably robust in conditions of strong energetic disorder, extreme physiological temperatures, and low light flux - very different from conventional solar conversion materials [1-3]. However, determining the key principles which are responsible for efficient conversion is a challenging task due to the complexity of the photosynthetic systems. The field encountered a fascinating lead in 2007 when oscillatory features were discovered in two-dimensional electronic spectroscopic data - the optical analogue of 2D NMR - and were assigned to quantum coherence between donor and acceptor electronic st...