Coherence in light harvesting

Quantum effects in photosynthesis

Light-harvesting apparatus of purple bacteria, where we have shown that supertransfer—a coherent effect caused by excitonic delocalisation—plays a critical role.16, 19

Photosynthetic organisms harvest light using antenna complexes containing many chlorophyll molecules. The harvested energy is then transported to reaction centres, where it drives the first chemical steps of photosynthesis. Recent experiments have suggested that the energy transport can be partially coherent, challenging assumptions that quantum effects could not be relevant in biological systems at room temperature.

We have shown that many of the quantum effects observed in photosynthetic complexes are side effects of the laser excitation and are not relevant to biological function in sunlight.11, 14 Therefore, describing energy transport in incoherent light can be dramatically simplified, allowing us to rapidly screen hypothetical scenarios to determine whether natural light-harvesting architectures are already optimal or whether they could be improved.16, 19

Our screening studies identified several quantum effects that are important even in incoherent light.16 In particular, we reported the most statistically significant quantum enhancement in a photosynthetic complex,19 showing that the light-harvesting apparatus of purple bacteria is more than five standard deviations more efficient than would be expected by chance, and that the enhancement is largely due to supertransfer, a cooperative enhancement of energy transfer due to delocalisation.

We also analysed the performance of reaction centres to understand why they adopted the dimeric structure that has been conserved over billions of years of evolution. We found that the most probable explanation for the dimerism is that it deepened the excitonic trap in the special pair, which could considerably improve the efficiency.28

Engineering coherence-enhanced light harvesting

Example of coherence-enhanced light harvesting: Coherent laser light (right) can induce excitonic coherence between the two donors (blue sites) that increases the efficiency of energy transfer to the acceptor (purple) compared to what would happen in otherwise identical incoherent light (left).26, 29, 32

We are applying the lessons from photosynthesis to the design of artificial coherence-enhanced light harvesters, in which the coherence of the excitons, vibrations, or photons could be engineered to improve the light-harvesting efficiency.

We classified all possible mechanisms of coherent efficiency enhancements,29, 39 including a previously unreported one, and clarified which mechanisms would be most useful and most easily engineered into light-harvesting devices. In particular, coherent enhancements of light harvesting can be made controllable in some cases26, 39 and external noise can, surprisingly, further increase the coherent enhancement.32

Our results provide a roadmap for the first conclusive demonstration of coherence-enhanced light harvester, in which coherence could be turned on and off to definitively confirm its functional role. We are working with experimental colleagues to realise this demonstration—stay tuned or come join us!

Related papers

“Light-harvesting efficiency cannot depend on optical coherence in the absence of orientational order”
Dominic M. Rouse, Adesh Kushwaha, Stefano Tomasi, Brendon W. Lovett, Erik M. Gauger, and Ivan Kassal
J. Phys. Chem. Lett. 15, 254 (2024).
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The coherence of light has been proposed as a quantum-mechanical control for enhancing light-harvesting efficiency. In particular, optical coherence can be manipulated by changing either the polarization state or the spectral phase of the light. Here, we show that, in weak light, light-harvesting efficiency cannot be controlled using any form of optical coherence in molecular light-harvesting systems and, more broadly, those comprising orientationally disordered subunits and operating on longer-than-ultrafast time scales. Under those conditions, optical coherence does not affect the light-harvesting efficiency, meaning that it cannot be used for control. Specifically, polarization-state control is lost in disordered samples or when the molecules reorient on the time scales of light harvesting, and spectral-phase control is lost when the efficiency is time-averaged over a period longer than the optical coherence time. In practice, efficiency is always averaged over long times, meaning that coherent optical control is only possible through polarization and only in systems with orientational order.
“Environmentally improved coherent light harvesting”
Stefano Tomasi, Dominic M. Rouse, Erik M. Gauger, Brendon W. Lovett, and Ivan Kassal
J. Phys. Chem. Lett. 12, 6143 (2021).
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Coherence-enhanced light harvesting has not been directly observed experimentally, despite theoretical evidence that coherence can significantly enhance light-harvesting performance. The main experimental obstacle has been the difficulty in isolating the effect of coherence in the presence of confounding variables. Recent proposals for externally controlling coherence by manipulating the light’s degree of polarization showed that coherent efficiency enhancements would be possible, but they were restricted to light-harvesting systems weakly coupled to their environment. Here, we show that increases in system–bath coupling strength can amplify coherent efficiency enhancements, rather than suppress them. This result dramatically broadens the range of systems that could be used to conclusively demonstrate coherence-enhanced light harvesting or to engineer coherent effects into artificial light-harvesting devices.
“Classification of coherent enhancements of light-harvesting processes”
Stefano Tomasi and Ivan Kassal
J. Phys. Chem. Lett. 11, 2348 (2020).
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Several kinds of coherence have recently been shown to affect the performance of light-harvesting systems, in some cases significantly improving their efficiency. Here, we classify the possible mechanisms of coherent efficiency enhancements, based on the types of coherence that can characterize a light-harvesting system and the types of processes these coherences can affect. We show that enhancements are possible only when coherences and dissipative effects are best described in different bases of states. Our classification allows us to predict a previously unreported coherent enhancement mechanism, where coherence between delocalized eigenstates can be used to localize excitons away from dissipation, thus reducing the rate of recombination and increasing efficiency.
“Why are photosynthetic reaction centres dimeric?”
Natasha Taylor and Ivan Kassal
Chem. Sci. 10, 9576 (2019).
One of the “Most popular 2018–2019 chemistry articles” in Chemical Science.
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All photosynthetic organisms convert solar energy into chemical energy through charge separation in dimeric reaction centres. It is unknown why early reaction centres dimerised and completely displaced their monomeric ancestors. Here, we discuss several proposed explanations for reaction-centre dimerism and conclude—with only weak assumptions about the primordial dimerisation event—that the most probable explanation for the dimerism is that it arose because it enhanced light-harvesting efficiency by deepening the excitonic trap, i.e., by enhancing the rate of exciton transfer from an antenna complex and decreasing the rate of back transfer. This effect would have outweighed the negative effect dimerisation would have had on charge transfer within the reaction centre. Our argument implies that dimerisation likely occurred after the evolution of the first antennas, and it explains why the lower-energy state of the special pair is bright.
“Coherent and controllable enhancement of light-harvesting efficiency”
Stefano Tomasi, Sima Baghbanzadeh, Saleh Rahimi-Keshari, and Ivan Kassal
Phys. Rev. A 100, 043411 (2019).
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Spectroscopic experiments have identified long-lived coherences in several light-harvesting systems, suggesting that coherent effects may be relevant to their performance. However, there is limited experimental evidence of coherence enhancing light-harvesting efficiency, largely due to the difficulty of turning coherences on and off to create an experimental control. Here we show that coherence can indeed enhance light harvesting and that this effect can be controlled. We construct a model system in which initial coherence can be controlled using the incident light and which is significantly more efficient under coherent, rather than incoherent, excitation. Our proposal would allow for an unambiguous demonstration of light harvesting enhanced by intermolecular coherence, as well as demonstrate the potential for coherent control of excitonic energy transfer.
“Geometry, supertransfer, and optimality in the light harvesting of purple bacteria”
Sima Baghbanzadeh and Ivan Kassal
J. Phys. Chem. Lett. 7, 3804 (2016).
One of 18 physical chemistry papers highlighted by ACS as “Outstanding Work from Authors in Australia”.
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The remarkable rotational symmetry of the photosynthetic antenna complexes of purple bacteria has long been thought to enhance their light harvesting and excitation energy transport. We study the role of symmetry by modeling hypothetical antennas whose symmetry is broken by altering the orientations of the bacteriochlorophyll pigments. We find that in both LH2 and LH1 complexes, symmetry increases energy transfer rates by enabling the cooperative, coherent process of supertransfer. The enhancement is particularly pronounced in the LH1 complex, whose natural geometry outperforms the average randomized geometry by 5.5 standard deviations, the most significant coherence-related enhancement found in a photosynthetic complex.
“Distinguishing the roles of energy funnelling and delocalization in photosynthetic light harvesting”
Sima Baghbanzadeh and Ivan Kassal
Phys. Chem. Chem. Phys. 18, 7459 (2016).
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Photosynthetic complexes improve the transfer of excitation energy from peripheral antennas to reaction centers in several ways. In particular, a downward energy funnel can direct excitons in the right direction, while coherent excitonic delocalization can enhance transfer rates through the cooperative phenomenon of supertransfer. However, isolating the role of purely coherent effects is difficult because any change to the delocalization also changes the energy landscape. Here, we show that the relative importance of the two processes can be determined by comparing the natural light-harvesting apparatus with counterfactual models in which the delocalization and the energy landscape are altered. Applied to the example of purple bacteria, our approach shows that although supertransfer does enhance the rates somewhat, the energetic funnelling plays the decisive role. Because delocalization has a minor role (and is sometimes detrimental), it is most likely not adaptive, being a side-effect of the dense chlorophyll packing that evolved to increase light absorption per reaction center.
“Benchmarking calculations of excitonic couplings between bacteriochlorophylls”
Elise Kenny and Ivan Kassal
J. Phys. Chem. B 120, 25 (2016).
One of 18 physical chemistry papers highlighted by ACS as “Outstanding Work from Authors in Australia”.
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Excitonic couplings between (bacterio)chlorophyll molecules are necessary for simulating energy transport in photosynthetic complexes. Many techniques for calculating the couplings are in use, from the simple (but inaccurate) point-dipole approximation to fully quantum-chemical methods. We compared several approximations to determine their range of applicability, noting that the propagation of experimental uncertainties poses a fundamental limit on the achievable accuracy. In particular, the uncertainty in crystallographic coordinates yields an uncertainty of about 20% in the calculated couplings. Because quantum- chemical corrections are smaller than 20% in most biologically relevant cases, their considerable computational cost is rarely justified. We therefore recommend the electrostatic TrEsp method across the entire range of molecular separations and orientations because its cost is minimal and it generally agrees with quantum-chemical calculations to better than the geometric uncertainty. Understanding these uncertainties can guard against striving for unrealistic precision; at the same time, detailed benchmarks can allow important qualitative questions—which do not depend on the precise values of the simulation parameters—to be addressed with greater confidence about the conclusions..
“Importance of excitation and trapping conditions in photosynthetic environment-assisted energy transport”
Roberto J. León-Montiel, Ivan Kassal, and Juan P. Torres
J. Phys. Chem. B 118, 10588 (2014).
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It has been argued that excitonic energy transport in photosynthetic complexes is efficient because of a balance between coherent evolution and decoherence, a phenomenon called environment-assisted quantum transport (ENAQT). Studies of ENAQT have usually assumed that the excitation is initially localized on a particular chromophore, and that it is transferred to a reaction center through a similarly localized trap. However, these assumptions are not physically accurate. We show that more realistic models of excitation and trapping can lead to very different predictions about the importance of ENAQT. In particular, although ENAQT is a robust effect if one assumes a localized trap, its effect can be negligible if the trapping is more accurately modeled as Forster transfer to a reaction center. Our results call into question the suggested role of ENAQT in the photosynthetic process of green sulfur bacteria and highlight the subtleties associated with drawing lessons for designing biomimetic light-harvesting complexes.
“Does coherence enhance transport in photosynthesis?”
Ivan Kassal, Joel Yuen-Zhou, and Saleh Rahimi-Keshari
J. Phys. Chem. Lett. 4, 362 (2013).
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Recent observations of coherence in photosynthetic complexes have led to the question of whether quantum effects can occur in vivo, not under femtosecond laser pulses but in incoherent sunlight and at steady state, and, if so, whether the coherence explains the high exciton transfer efficiency. We distinguish several types of coherence and show that although some photosynthetic pathways are partially coherent processes, photosynthesis in nature proceeds through stationary states. This distinction allows us to rule out several mechanisms of transport enhancement in sunlight. In particular, although they are crucial for understanding exciton transport, neither wavelike motion nor microscopic coherence, on their own, enhance the efficiency. By contrast, two partially coherent mechanisms—ENAQT and supertransfer—can enhance transport even in sunlight and thus constitute motifs for the optimisation of artificial sunlight harvesting. Finally, we clarify the importance of ultrafast spectroscopy in understanding incoherent processes.
“Environment-assisted quantum transport”
Patrick Rebentrost, Masoud Mohseni, Ivan Kassal, Seth Lloyd, and Alán Aspuru-Guzik
New J. Phys. 11, 033003 (2009).
Selected “Best of 2009” by New J. Phys., one of six papers in quantum physics.
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Transport phenomena at the nanoscale are of interest due to the presence of both quantum and classical behavior. In this work, we demonstrate that quantum transport efficiency can be enhanced by a dynamical interplay of the system Hamiltonian with pure dephasing induced by a fluctuating environment. This is in contrast to fully coherent hopping that leads to localization in disordered systems, and to highly incoherent transfer that is eventually suppressed by the quantum Zeno effect. We study these phenomena in the Fenna–Matthews–Olson protein complex as a prototype for larger photosynthetic energy transfer systems. We also show that the disordered binary tree structures exhibit enhanced transport in the presence of dephasing.