Photosynthetic Energy Transfer at the Quantum/Classical Border

Highlights

Quantum mechanics diverges from the classical description of our world when very small scales or very fast processes are involved. Unlike classical mechanics, quantum effects cannot be easily related to our everyday experience and are often counterintuitive to us. Nevertheless, the dimensions and time scales of the photosynthetic energy transfer processes puts them close to the quantum/classical border, bringing them into the range of measurable quantum effects. Here we review recent advances in the field and suggest that photosynthetic processes can take advantage of the sensitivity of quantum effects to the environmental ‘noise’ as means of tuning exciton energy transfer efficiency. If true, this design principle could be a base for ‘nontrivial’ coherent wave property nano-devices.

Quantum Theory Describes Our World

Quantum mechanics is the cornerstone of modern physics and chemistry. All experiments done so far show that, while many aspects of quantum mechanics are counterintuitive and seem paradoxical, the description of quantum behavior is correct. An example of this is the famous double-slit experiment, which demonstrated that a single electron could travel in two paths and create an interference pattern with itself. This experiment validated the wave/particle duality concept, a key concept in quantum mechanics that will also play an important role in this review.

While quantum effects direct the mechanics of atoms and electrons, it is important to remember that the number of particles in a given volume increases with the cube of its radius, so going from 0.5 nm (a small molecule) to 5 nm (a typical protein) brings into play a thousand times more atoms. These dimensions place an explicit quantum simulation of a biological process beyond the reach of calculating power of current computers.

Nevertheless, quantum effects in biology are evident in daily life. Two major concepts of quantum mechanics govern their operation. The first is the quantized behavior of physical properties like energy and momentum. A simple demonstration is related to quantized energy levels (see Glossary) confined in small chemical structures. For example, a pigments’ absorption spectrum (Box 1) or Förster resonance energy transfer (FRET) (Box 2) between pigments.

Identifying the Fingerprints of Quantum Effects in Photosynthesis

Probing ultrafast processes requires sophisticated spectroscopic tools, such as 2D electron spectroscopy (2DES) [12345]. The introduction of these techniques to the study of photosynthetic EET processes resulted in the suggestion that coherent transfer could be detected in a small soluble antenna protein of a green sulfur photosynthetic bacterium containing eight pigments (the FMO protein) [6]. This was a revolutionary hypothesis, since for many years these EET processes were described by the more basic FRET energy transfer equations. FMO transports excitons from one end to another via eight chlorophyll molecules embedded in the protein, like currants in a bun. The small number of pigments in this protein made it an ideal test case for a 2DES study (for insight into 2DES methodology and its importance in biological and chemical quantum studies, see the recent review by Scholes and coworkers [4]). In photosynthesis, the picture that has emerged from these studies provides a remarkably detailed map of the dynamics of the EET process [78].

According to the coherent interpretation of the data, the exciton does not usually reside on a single chlorophyll, but is spread over several chromophores, creating a wave packet [910111213]. In this scenario, the phase of the wave packetbecomes important (Box 3). Dealing with waves, EET will be controlled by constructive and destructive interference patterns. In other words, changing phase differences between packets will control EET rates. This manifests itself as ‘beats’ in the rate of exciton transfer as the different paths interfere.

Since this original discovery, evidence for quantum coherent effects were reported for a number of photosynthetic LH and RC pigment–protein complexes (examples include [14151617181920212223242526]). However, it is important to note that the interpretation of these 2DES results is still debated. The beats in the 2DES spectra could be either due to true electronic coherences, where the beats are created by the quantum properties of the wave packet while energy is transferred, indicating the involvement of coherent wave packets. Alternatively, they could be due to coupling of the excitation to mechanical vibrations of the protein. The energies involved in exciting an electron from a ground state to an excited state in a photosynthetic pigment are large, of the order of 2 electron-volts. Molecular vibration energies of proteins take place at energies 10–100 times smaller. This means that the electron excitation could transfer energy to the vibrations, and these could in turn modulate electron transfer, thereby giving rise to beats without the need to invoke quantum coherence [272829].

A major challenge in this field is therefore to identify the contributions of incoherent and quantum coherent processes.

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