International Symposium "Nanoscience and Quantum Physics 2011" Journal of Physics: Conference Series 302 (2011) 012037

IOP Publishing doi:10.1088/1742-6596/302/1/012037

Quantum coherence in biological systems

Seth Lloyd
Department of Mechanical Engineering, MIT Abstract. This paper reviews the role of quantum mechanics in biological systems, and shows how the interplay between coherence and decoherence can strongly enhance quantum transport in photosynthesis.

Nature is the great nano-technologist. The chemical machinery that powers biological systems consists of complicated molecules structured at the nanoscale and sub-nanoscale. At these small scales, the dynamics of the chemical machinery is governed by the laws of quantum mechanics. Quantum mechanics is well known to exhibit strange and counterintuitive eects. Accordingly, it makes sense to investigate the extent to which peculiarly quantum eects such as coherence and entanglement play an important role in living systems. Quantum mechanics and quantum coherence play a central role in chemistry. Quantum coherence and entanglement determine the valence structure of atoms and the form of covalent bonds. Quantum mechanics xes the set of allowed chemical compounds and sets the parameters of chemical reactions. Indeed, the very fact that there are only a countable, discrete set of possible chemical compounds arises from the fundamentally discrete nature of quantum mechanics. Chemistry, in turn, lays down the rules for what biological structures are possible and for how they function. Biomolecules can contain many atoms (billions in the case of DNA). As molecules become larger and more complex, quantum coherence becomes harder to maintain. Vibrational modes and interactions with the environment tend to decohere quantum superpositions. Consequently, most biomolecular mechanisms have traditionally been modeled as essentially classical processes. For example, classical ball and spring models of molecules can capture accurately many aspects of molecular dynamics. As a result, for many years, the conventional answer to the question of whether quantum coherence and entanglement are important for biological processes has been, not really. Recently, however, strong evidence has emerged that quantum coherence is playing an important role in certain selected biological processes [1-3]. The strongest evidence for quantum coherence occurs in photosynthesis, which will form the main topic of this paper (a review of the mechanisms for photosynthesis can be found in [4]. Indirect evidence for quantum coherence also appears in bird navigation [5-6] the so-called avian compass and in the sense of smell [7-8]. Before turning to photosynthesis, I will review the evidence for quantum eects in these biological mechanisms. (1) The avian compass. Some birds, such as homing pigeons, possess a small piece of magnetite in their beaks which functions as a compass, allowing them to tell North from South. Other birds, such as the European robin, seem to possess a dierent mechanism for sensing the earths magnetic eld [5-6]. This mechanism (a) allows the birds to identify the angle the magnetic
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International Symposium "Nanoscience and Quantum Physics 2011" Journal of Physics: Conference Series 302 (2011) 012037

IOP Publishing doi:10.1088/1742-6596/302/1/012037

eld lines make with the earth, but does not distinguish North from South; (b) is only activated in blue or green light; and (c) is disrupted by oscillating elds a bit above one megahertz, at the electrons Larmor frequency in the earths magnetic eld. These features are dicult to explain using classical mechanisms. The only known mechanism consistent with these features is quantum mechanical. The proposed mechanism postulates that absorption of blue or green light creates a radical pair of electrons, separated within an oriented molecule (perhaps a cryptochrome) within the birds eye. The racial pair undergoes coherent quantum oscillations between entangled singlet and triplet states, at a rate that depends on the orientation of the host molecule with respect to the earths magnetic eld. A spin-dependent electron transition then allows current to ow only if the spins in the pair are in a particular symmetry state. The rate of current ow then depends on the molecules relative orientation to the eld. This purely quantum mechanical mechanism explains all peculiar observed features of the birds behavior, including their inability to tell North from South. Ongoing experimental and theoretical investigations are attempting to identify the molecules or molecular complexes within which this mechanism can function, and to devise detailed and testable models for its operation. (2) Sense of smell. The conventional mechanism postulated for smell is a lock and key model, in which dierent types of odorant molecule bind to dierent types of olfactory sensors. The dierent types of olfactory sensors in the human nose have been identied. In this model, the particular smell of an odorant molecule depends only on its anity to dierent sensors. There are several issues with this model. First of all, the smell of a molecule depends at most weakly on shape, the primary determinant of the sensors to which the molecule binds in a lock and key model. Second, smell correlates well with the vibrational spectrum of the molecule: for example, a sulphur-less molecule whose vibrational spectrum exhibits a resonance at the same frequency as the sulphur-hydrogen stretch mode, smells of sulphur. The nose is evidently a vibrational spectrometer. Again, the only known mechanism that can explain this vibrational sensitivity of the sense of smell is quantum mechanical [7-8]. The mechanism relies on inelastic tunneling. Once an odorant molecule docks into the olfactory sensor, electrons can pass through the molecule, and current can ow, only by emitting a phonon of specic frequency to one of the molecules dominant vibrational modes. The strongest conrming evidence for this mechanism is the ability of fruit ies (drosophila) to smell the dierence between an organic molecule and a deuterated version of the same molecule. A molecule whose hydrogens have been replaced by deuterium should bind to the same receptors as the original molecule, with similar anities. So if the shapebased lock and key mechanism were true, it should smell the same. By contrast, deuterium carbon bonds vibrate at a rate 2 slower than hydrogen-carbon bonds: deuteration signicantly changes the vibrational spectrum of the molecule. Ongoing work to validate further this purely quantum mechanical mechanism includes performing X-ray crystallography to identify the precise geometry of the receptor molecules, and creating detailed quantum mechanical models to test and elucidate the specic mechanisms of inelastic tunneling. Photosynthesis. I now turn to quantum coherence in photosynthesis, the primary topic of this article. In the cases of the avian compass and sense of smell just described, the primary evidence for quantum eects is observation of animal behavior, combined with a lack of plausible classical models. By contrast, in photosynthesis, the evidence for the eects of quantum coherence is direct and overwhelming [1-3]. In photosynthesis, a particle of light or photon is absorbed by a photocomplex, a set of molecular structures embedded in the membrane of a plant or bacterial cell. Part of the energy of the photon is converted into heat in the form of molecular vibrations, but most of it is

International Symposium "Nanoscience and Quantum Physics 2011" Journal of Physics: Conference Series 302 (2011) 012037

IOP Publishing doi:10.1088/1742-6596/302/1/012037

captured as an exciton, a bound electron-hole pair that resides in a chromophore, a lightcarrying molecule such as a plant or bacterial chlorophyll. The exciton is so-called Frenkel exciton, tightly bound within a region a few angstroms on each side. Energy transfer occurs via the dipolar interaction between chromophores: a so-called Frster coupling between induced o or transition dipoles de-excites one chromophore while exciting a neighboring one. The exciton must propagate through hundreds or thousands of chromophores in order to reach the reaction center, a special molecular complex in which charge separation takes place. The exciton transport process is, of course, governed by the laws of quantum mechanics. For decades, however, this process was thought to be minimally quantum mechanical, in the sense that while quantum mechanics determined couplings between chromophores, the actual transition rates could be calculated semi-classically using Fermis golden rule. In 2007, this picture changed dramatically when the Fleming group in Berkeley used femtosecond twodimensional spectroscopy based on four-wave mixing to demonstrate that quantum coherence was at work the transfer process. The spectroscopic signature exhibited clear evidence of quantum beating at 77K, a result that was later conrmed at room temperature. The evidence for quantum coherence in photosynthetic transport was essentially incontrovertible. My own background is in quantum computation, not photochemistry. I became involved in this eld completely by accident. When the Fleming paper came out, the New York Times reported it as claiming that green sulphur bacteria were performing a quantum computation. Quantum computers are devices that use quantum coherence to process information in ways that classical computers can not. Specic methods for performing a quantum computation are called quantum algorithms. The Fleming paper speculated that the demonstrated coherence in excitonic transport meant that bacteria were performing a quantum algorithm called quantum search to allow the exciton to travel from the place and to nd the reaction center. This claim caused great hilarity in our quantum information theory group at MIT, as it seemed implausible that a quantum algorithm such as quantum search could be performed in the hot, wet, and noisy conditions inside a living cell. Despite our collective skepticism, conscientiousness obliged us to take a look. Moreover, Alan Aspuru-Guzik, an assistant professor of chemistry at Harvard, had interacted with the Fleming group and could vouch for the seriousness and accuracy of their results. So I read the paper and discussed it with Alan. The paper was a masterwork. The evidence for quantum coherence was exceptionally strong. The line about quantum search algorithms was essentially an afterthought. Quantum search algorithms, invented by Lov Grover in 1996, take a unique form [9]: we were able to show right away that the bacteria were not performing a quantum search algorithm. To our surprise, however, the bacteria were in fact performing a dierent type of quantum algorithm, called a quantum walk. A random walk is a transport mechanism in which the walker takes steps in random directions through the network or structure to be traversed. In a classical random walk, the position of the walker gradually diuses throughout the network. Because the walker is equally likely to move in any direction, after time t the walker has moved from its original position by an distance proportional to t. In a quantum walk, by contrast, the walker takes a quantum superposition of paths through the network [10]. These paths can exhibit quantum interferences. If the interference is destructive, the walker becomes stuck or localized within the network. By contrast, if the interference is constructive, the walker moves from its original position by a distance proportional to t, a considerable improvement over the classical random walk. The coherence demonstrated by the Fleming group showed that the excitons were performing a quantum walk, at least over short distances. Excited, we decided to make a detailed quantum mechanical model of the excitonic transport process, a model that took into account the strong role of quantum coherence. We were aided by the fact that the quantum structure of the particular photosynthetic complex on which

International Symposium "Nanoscience and Quantum Physics 2011" Journal of Physics: Conference Series 302 (2011) 012037

IOP Publishing doi:10.1088/1742-6596/302/1/012037

Fleming had performed his experiment was well-known. The Fenna-Matthews-Olsen complex, or FMO, had been exhaustively studied using both spectroscopy and by X-ray crystallography [1-3]. Consequently, we were able to make a full quantum model of the dynamics of excitonic transport through the complex, including its interaction with the environment. Because of the well-studied nature of the complex, the only free parameter in our model was the temperature, which we could vary at will. All other parameters in the model were determined by pre-existing experiments. When Alans postdoc, Masoud Mohseni, and graduate student Patrick Rebentrost coded the model into a computer and red it up, we found that the eciency of excitonic transport had a remarkable dependence on temperature [11-12]. (Subsequently but independently, Martin Plenio and co-workers at Imperial College developed a similar model which conrmed this behavior [13].) At low temperatures, the interference between paths in the excitonic walk was predominantly destructive, localizing the exciton to within a few sites of its initial position. At higher temperatures, however, the interaction with the environment decohered the quantum walk suciently to remove that destructive interference, allowing the exciton to diuse throughout the FMO complex towards the reaction center. At very high temperatures, the decoherence induced by the environment was so destructive that it froze the exciton in place, reducing the eciency of the transport. The highest eciency for transport was 290K, the average temperature of the water in which the bacteria lived. Moreover, the transport was robust with respect to variation about this optimal temperature, exhibiting almost 100% eciency for a range of many tens of degrees K in both directions. Our model gave a clear picture of the role of quantum coherence in excitonic transfer in FMO: quantum coherence allowed the exciton to spread rapidly and coherently over a small number of sites, then environmentally induced decoherence kicked in to prevent the exciton from being localized. The transport eciency exhibited a distinctive signature as a function of temperature low at low temperature, high for a range around some optimum temperature, then low again at high temperature. Because this particular signature was a function not of the individual system under investigated, but of any partially coherent transport process, we gave it the name ENAQT for Environmentally Assisted Quantum Transport. ENAQT applies to essentially any type of partially coherent quantum transport through a disordered medium. In addition, our model gave insight into the evolutionary mechanism underlying a phenomenon that had puzzled photochemists and biologists for decades the convergence of time scales in photosynthesis. Separation of time scales is a common phenomenon in physical systems. The initial absorption of a photon and creation of an exciton in a chromophore is a fast process, taking only a few femtoseconds. By contrast, the exciton lives for several nanoseconds before decaying. So there is a six order of magnitude separation of time scales between absorption and decay. The physiological benets of this particular separation of time scales is easy to see: fast absorption arises from strong coupling of the chromophore to light, and to absorption over a broad band of frequencies, both desirable characteristics. Long lifetimes increase the chance that the exciton will make it to the reaction center. All other time scales in the excitonic transport process, however coupling constants, energy dierences, decoherence rates, and environmental correlation times converged to the scale of a picosecond or so. Why? The convergence of time scales makes excitonic transport in photosynthesis hard to model. When time scales are separated, dierent processes at dierent time scales can be modeled accurately as perturbation to an underlying process. When time scales converge, no simple model is possible. So one explanation of why time scales converge is that Nature is modest and prefers not to reveal her secrets to scientists. A more physical explanation is that when time scales for dierent processes converge, the strong interaction between the processes can either help transport, or hurt it. In systems that have undergone a billion years of natural selection, it should come as little surprise that these temporally convergent processes help each other out.

International Symposium "Nanoscience and Quantum Physics 2011" Journal of Physics: Conference Series 302 (2011) 012037

IOP Publishing doi:10.1088/1742-6596/302/1/012037

To test this hypothesis, we varied the parameters in our model to test the eciency of transport in non-physiological regimes where the time scales for dierent processes were not the same [14]. These studies showed that when time scales failed to converge, the eciency of transport was lower. We call this eect the quantum Goldilocks eect after the little girl in the folk tale who enters a house in which there is three of everything three chairs, three beds, three bowls of porridge on the table. One of the chairs is too large, one too small, and one is just the right size. So Goldilocks sits on the chair that is just right. One of the bowls of porridge is too cold, one too hot, and the third is just the right temperature. So she eats that one. Finally, she falls asleep on the bed that has just the right degree of softness. (At this point, the three bears who live in the house return home and become upset, but that is another story.) The Goldilocks eect natural selection chooses just the right degree for each eect is well known in biology. There is also a Goldilocks principle for complexity of evolved or designed systems [15]: too little complexity compromises function, while too much complexity diminishes robustness. Well-designed or well-evolved systems typically exhibit just the right degree of complexity. In the quantum Goldilocks eect, natural selection has made time scales converge, adding between quantum processes in photosynthesis until photosynthetic systems attain just the right degree of quantum complexity. Our simulations that vary the dierent parameters of the FMO complex show that the FMO complex has attained just the right degree of quantum complexity to give essentially 100% eciency while remaining robust. Conclusion: Quantum coherence plays a strong role in photosynthetic energy transport, and may also play a role in the avian compass and sense of smell. In retrospect, it should come as no surprise that quantum coherence enters into biology. Biological processes are based on chemistry, and chemistry is based on quantum mechanics. If an organism can attain an advantage in reproduction, however slight, by putting quantum coherence to use, then over time natural selection has a chance to engineer the necessary biochemical mechanisms to exploit that coherence. Dierent types of quantum processes that operate at the same time scale can interact strongly either to assist or to impede one another. In photosynthetic energy transfer, the convergence of quantum time scales gives rise to more ecient and robust transport. Evolved biological systems exhibit the quantum Goldilocks eect: natural selection pushes together time scales to allow quantum processes to help each other out. References
[1] Engel G S, Calhoun T R, Read E L, Ahn T K, Mancal T, Cheng Y C, Blankenship R E and Fleming G R 2007 Nature 446 782 [2] Collini E, Wong C Y, Wilk K E, Curmi P M, Brumer P and Scholes G D 2010 Nature 463 644 [3] Panitchayangkoon G, Hayes D, Fransted K A, Caram J R, Harel E, Wen J, Blankenship R E and Engel G S 2010 Proc. Nat. Acad. Sci. 107 12766 [4] Blankenship R E 2002 Molecular Mechanisms of Photosynthesis, (London: Blackwell Science) [5] Ritz T, Adem S and Schulten K 2000 Biophys. J. 78 707 [6] Rodgers T and Hore P J 2009 Proc. Nat. Acad. Sci. USA 106 353 [7] Turin L 1996 Chem. Senses 21 773 [8] Franco M I, Turin L, Mershin A and Skoulakis E M C 2011 Proc. Nat. Acad. Sci. USA 108 3797 [9] Grover L K 1996 Proc. 28th Ann. ACM Sym. Th. Comp. p 212 [10] Farhi E and Gutmann S 1998 Phys. Rev. A 58 915 [11] Mohseni M, Rebentrost P, Lloyd S and Aspuru-Guzik A 2008 J. Chem. Phys. 129 174106 [12] Rebentrost P, Mohseni M, Kassal I, Lloyd S and Aspuru-Guzik A 2009 New J. Phys. 11 033003 [13] Plenio M B and Huelga S F 2008 New J. Phys. 10 113019 [14] Shabani A, Mohseni M, Rabitz H and Lloyd S 2011 (in preparation) [15] Lloyd S, lecture at Santa Fe Institute, 1990, as reported by Gell-Mann M The Quark and the Jaguar, 1994 (New York: A. Knopf)