Quantum coherence spectroscopy reveals complex dynamics in bacterial light-harvesting complex 2 (LH2)

Harel, Elad; Engel, Gregory S.

doi:10.1073/pnas.1110312109

Cited by 179 publications

(221 citation statements)

References 52 publications

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“…Thus, we conclude that, based on this initial analysis, the unique Trp network within an individual tubulin dimer can possess significant dipolar couplings capable of supporting quantum coherent beating effects similar to those observed in the FMO photosynthetic complex [4,5], LHCII [7,8], LH2 [9,10] and phycobiliprotein LHCs [11,12]. Furthermore, our results suggest that this network may support coherent energy transfer at physiological temperature between clusters of Trps in tubulin, and microtubule structures.…”

Section: Resultsmentioning

confidence: 68%

“…This limit was further pushed to 277 K, nearing physiological temperature, and effectively ruling out the 'warm and wet' limit for quantum phenomena in biology [5]. Furthermore, these coherent effects do not seem to be restricted to the FMO complex alone, and have been shown for LHCs in plants (LHCII) [6][7][8], bacteria (LH2) [9,10] and phycobiliproteins [11,12].…”

Section: Introductionmentioning

confidence: 99%

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The feasibility of coherent energy transfer in microtubules

Craddock

Friesen

Mane

et al. 2014

J. R. Soc. Interface.

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It was once purported that biological systems were far too 'warm and wet' to support quantum phenomena mainly owing to thermal effects disrupting quantum coherence. However, recent experimental results and theoretical analyses have shown that thermal energy may assist, rather than disrupt, quantum coherent transport, especially in the 'dry' hydrophobic interiors of biomolecules. Specifically, evidence has been accumulating for the necessary involvement of quantum coherent energy transfer between uniquely arranged chromophores in light harvesting photosynthetic complexes. The 'tubulin' subunit proteins, which comprise microtubules, also possess a distinct architecture of chromophores, namely aromatic amino acids, including tryptophan. The geometry and dipolar properties of these aromatics are similar to those found in photosynthetic units indicating that tubulin may support coherent energy transfer. Tubulin aggregated into microtubule geometric lattices may support such energy transfer, which could be important for biological signalling and communication essential to living processes. Here, we perform a computational investigation of energy transfer between chromophoric amino acids in tubulin via dipole excitations coupled to the surrounding thermal environment. We present the spatial structure and energetic properties of the tryptophan residues in the microtubule constituent protein tubulin. Plausibility arguments for the conditions favouring a quantum mechanism of signal propagation along a microtubule are provided. Overall, we find that coherent energy transfer in tubulin and microtubules is biologically feasible.

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Section: Resultsmentioning

confidence: 68%

Section: Introductionmentioning

confidence: 99%

The feasibility of coherent energy transfer in microtubules

Craddock

Friesen

Mane

et al. 2014

J. R. Soc. Interface.

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“…Various models addressed the high efficiency of energy transfer in photosynthetic antennae (14)(15)(16)(17)(18)(19) and the mechanisms of charge separation in reaction centers (12,(20)(21)(22). Furthermore, quantum coherence effects, e.g., photon echo, have been observed in a series of interesting photosynthesis experiments (23)(24)(25)(26)(27)(28)(29)(30). Oscillations of exciton population signals in the 2D photon echo (rephasing) spectra have been predicted (31) and directly observed (32) as evidence of quantum transport.…”

mentioning

confidence: 99%

Photosynthetic reaction center as a quantum heat engine

Dorfman

Voronine

Mukamel

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

272

339

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Two seemingly unrelated effects attributed to quantum coherence have been reported recently in natural and artificial light-harvesting systems. First, an enhanced solar cell efficiency was predicted and second, population oscillations were measured in photosynthetic antennae excited by sequences of coherent ultrashort laser pulses. Because both systems operate as quantum heat engines (QHEs) that convert the solar photon energy to useful work (electric currents or chemical energy, respectively), the question arises whether coherence could also enhance the photosynthetic yield. Here, we show that both effects arise from the same population-coherence coupling term which is induced by noise, does not require coherent light, and will therefore work for incoherent excitation under natural conditions of solar excitation. Charge separation in light-harvesting complexes occurs in a pair of tightly coupled chlorophylls (the special pair) at the heart of photosynthetic reaction centers of both plants and bacteria. We show the analogy between the energy level schemes of the special pair and of the laser/photocell QHEs, and that both population oscillations and enhanced yield have a common origin and are expected to coexist for typical parameters. We predict an enhanced yield of 27% in a QHE motivated by the reaction center. This suggests nature-mimicking architectures for artificial solar energy devices.photosynthesis | quantum biology | population oscillations | quantum coherence A ccording to the laws of quantum thermodynamics, quantum heat engines (QHEs) convert hot thermal radiation into low-entropy useful work (1, 2). The ultimate efficiency of such QHEs is usually governed by a detailed balance between absorption and emission of the hot pump radiation (3). The laser is an example of a QHE, which can use incoherent pump (heat) radiation to produce highly coherent (low-entropy) light ( Fig. 1 A and B). Moreover, it was demonstrated both theoretically and experimentally that noise-induced quantum coherence (4) can break detailed balance and yield lasers without population inversion (5) and/or with enhanced efficiency (Fig. 1C).Recently it has been shown that quantum coherence can, in principle, enhance the efficiency of a solar cell or a photodetector (6-10). This photocell QHE (Fig. 1D) can be described by the same model as the laser QHE (Fig. 1E) and obeys similar detailed balance physics. To use the broad solar spectrum and eliminate phonon loss, we separate solar flux into narrow frequency intervals and direct it onto a cell array where each of the cells has been prepared to have its band gap equal to that photon energy (7). In particular, Shockley and Queisser (11) invoked detailed balance to show that the open-circuit voltage of a photocell is related to the energy input of a "hot" monochromatic thermal light by the Carnot factor. However, just as in the case of the laser, we can, in principle, break detailed balance by inducing coherence (Fig. 1F), which can enhance the photocell efficiency (9, 10).Other recent p...

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“…Finally, we note that increasingly sophisticated techniques continue to yield exciting discoveries at the molecular level of LH2 (27). Although we have here considered only the EET between individual LH2 complexes, thus ignoring the dynamics that occur within the complex, our qualitative conclusions should remain intact.…”

Section: Discussionmentioning

confidence: 99%

Optimal fold symmetry of LH2 rings on a photosynthetic membrane

Cleary

Chen

Chuang

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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An intriguing observation of photosynthetic light-harvesting systems is the N-fold symmetry of light-harvesting complex 2 (LH2) of purple bacteria. We calculate the optimal rotational configuration of N-fold rings on a hexagonal lattice and establish two related mechanisms for the promotion of maximum excitation energy transfer (EET). (i) For certain fold numbers, there exist optimal basis cells with rotational symmetry, extendable to the entire lattice for the global optimization of the EET network. (ii) The type of basis cell can reduce or remove the frustration of EET rates across the photosynthetic network. We find that the existence of a basis cell and its type are directly related to the number of matching points S between the fold symmetry and the hexagonal lattice. The two complementary mechanisms provide selection criteria for the fold number and identify groups of consecutive numbers. Remarkably, one such group consists of the naturally occurring 8-, 9-, and 10-fold rings. By considering the inter-ring distance and EET rate, we demonstrate that this group can achieve minimal rotational sensitivity in addition to an optimal packing density, achieving robust and efficient EET. This corroborates our findings i and ii and, through their direct relation to S, suggests the design principle of matching the internal symmetry with the lattice order.P hotosynthesis lies at the heart of all life on the planet. Excitation energy created in a peripheral light-harvesting antenna complex, upon absorption of a photon, is efficiently transferred via an exciton mechanism, sometimes over hundreds of angstroms, to a reaction center where charge separation takes place, creating a transmembrane electrochemical potential difference that ultimately drives the production of ATP. Light-harvesting antenna complexes, whose primary function is to increase the effective crosssection for photon absorption, while maintaining an efficient energy transfer network, consist of well-ordered membrane-associated arrays of light-absorbing pigments, namely chlorophyll or bacterichlorophyll (BChl), embedded in a protein environment (1-4).Perhaps the most intriguing aspect of light-harvesting systems is the N-fold symmetry displayed by light-harvesting complex 2 (LH2) of purple nonsulfur bacteria. Fold symmetry occurs in systems as diverse as carbon nanotubes, tubular dye aggregates, and the mosaic virus protein, as well as in snow flakes, tori, and nonperiodic tilings (5). In LH2, the N-fold symmetry arises from the N repetitions of a basic heterodimer subunit consisting of two transmembrane polypeptides, α and β, arranged in a circular structure (6-8). Each αβ-heterodimer subunit noncovalently binds one B800 BChl and two B850 BChls (Fig. 1A), so named according to their respective room-temperature absorption bands in the infrared region of the spectrum. In most bacterial species, the αβ-heterodimer repeats eight or nine times to form an octameric or nonameric ring structure (in Rhodopseudomonas paulisterium 10-fold rings have also been observ...

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Quantum coherence spectroscopy reveals complex dynamics in bacterial light-harvesting complex 2 (LH2)

Cited by 179 publications

References 52 publications

The feasibility of coherent energy transfer in microtubules

The feasibility of coherent energy transfer in microtubules

Photosynthetic reaction center as a quantum heat engine

Optimal fold symmetry of LH2 rings on a photosynthetic membrane

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