The photosynthetic apparatus of cryptophyte algae is odd — its pigments are farther apart than is expected for efficient functioning. A study into how this apparatus works so well finds quantum effects at play.

It is common knowledge that plants, algae and certain bacteria use photosynthesis to convert solar energy into a form that can be used by the organisms to live and reproduce. But what is less well known is that the efficiency of photosynthesis might depend in part on quantum-mechanical processes. On page 644 of this issue, Collini et al.1 report evidence suggesting that a process known as quantum coherence 'wires' together distant molecules in the light-harvesting apparatus of marine cryptophyte algae. This is the first time that this phenomenon has been observed in photosynthetic proteins at room temperature, rather than at much lower temperatures, bolstering the idea that quantum coherence influences light harvesting in vivo.

At a molecular level, the light-harvesting proteins (antennas) of photosynthetic organisms absorb solar photons, which excite electrons in pigment molecules. The antennas guide the resulting excitation energy to complexes of proteins known as reaction centres. The excited reaction centres then drive an ultrafast charge-separation process across a membrane, initiating a host of biochemical events that generate chemical energy. Remarkably, the energy transfer from the antennas to the reaction centre is almost perfectly efficient2.

But why are light-harvesting antennas needed at all? Couldn't the reaction centres simply respond directly to incoming photons? There are several answers to these questions. First, photosynthesis must be able to operate at low light levels, such as those that generate less than one electronic excitation per molecule of chlorophyll per second. Yet the most important biochemical reactions associated with photosynthesis require several electron-transfer events. For example, water oxidation — a light-induced reaction in which water molecules split apart to generate protons, electrons and oxygen — requires the cumulative effect of four electronic excitations, all of which must occur within a certain time. Antennas overcome this problem by concentrating the available light energy, feeding the electronic excitations from hundreds of light-absorbing pigment molecules into a single reaction centre.

Another reason for having antennas is that they allow photosynthetic organisms to survive using fewer reaction centres. This is beneficial because reaction centres are 'expensive' — each one requires a large investment of resources from the host organism. Antennas also allow a broad range of the spectrum to be exploited for photosynthesis, because antennas that contain different pigments (and which therefore absorb different colours of light) can be connected to one reaction centre.

Finally, in a multi-protein light-harvesting antenna, the flow of excitation energy can be regulated by modulating the quenching properties of one of the constituent proteins. This provides a way of protecting plants from potentially harmful absorbed energy from excess sunlight3.

So what is it that makes the light-harvesting process so efficient? There are many contributing factors. The first is that the pigments in light-harvesting complexes are optimally spaced — just closely enough to enable fast energy transfer2, but far enough apart to prevent the molecular orbitals of the pigments from overlapping, which would quench their excited states (a phenomenon known as concentration quenching)4. The second factor is the supramolecular organization of the photosynthetic apparatus, which allows a multitude of energy-delivery pathways to connect to the reaction centre5. Collini et al.1 now suggest that quantum coherence could be a third factor in optimizing energy-transfer efficiency.

The authors investigated two kinds of antenna complex taken from cryptophyte algae. Cryptophyte antennas exhibit exceptional spectral variation between species, largely because the structure of their main light-harvesting pigment (bilin) can be tuned to absorb different light frequencies. The authors excited the complexes using a short laser pulse (25 femtoseconds; 1 fs is 10−15 seconds), thus creating a superposition of excited electronic states known as a wavepacket, which evolves in time according to the laws of quantum mechanics. These laws predict that the wavepacket will behave in an oscillatory manner between the positions at which the excitation is localized, with distinct correlations and anti-correlations in phase and amplitude6, 7, analogous to a collection of oscillating pendulums connected by weak springs. This coherent, collective behaviour would eventually disappear because of interactions between the individual excited pigments and their 'noisy' protein environment.
 

Such oscillatory behaviour in response to laser excitation has been observed before8 in the light-harvesting complex of green sulphur bacteria. However, those experiments were performed at cryogenic temperatures, at which the interaction of excited pigments with their environment is generally much smaller than at room temperature.

Collini et al.1 measured oscillating excitation dynamics in their algal antenna complexes using a technique called two-dimensional photon-echo spectroscopy. In this technique, the antenna under study is excited using a pair of short laser pulses, thus populating the different electronic levels of the system and creating electronic coherences (wave-like behaviour) between the different levels. The evolution of the excited state is then measured by following the spectral response of the 'photon echo' — emitted light that is induced by a delayed third pulse. By plotting the emission wavelength as a function of the excitation wavelength, a two-dimensional spectrum is obtained. The extent to which exciting the system at one frequency provokes the appearance of another frequency in the emission spectrum directly reflects the degree of coupling between pigments.

Collini et al. not only observed pronounced oscillations in the diagonal peaks and off-diagonal cross-peaks of their spectra, as would be expected if quantum coherence occurred in the antenna, but they also found that the lifetime of these oscillations was surprisingly long (more than 400 fs; lifetimes of less than 100 fs were expected). What's more, the coherences occurred between pigments that are distant from each other, and so weakly coupled. Such an effect was also recently suggested to occur between the weakly coupled pigments of bacterial light-harvesting complexes9, 10.

Long-lived quantum coherences in a bacterial light-harvesting complex have previously been observed8, but these were seen only at cryogenic (<77 kelvin) temperatures. By contrast, Collini and colleagues' experiments1 were performed at room temperature, suggesting that long-lived quantum coherence might have a role in real-world light-harvesting processes.

If so, what could this role be? The correlated wave-like motion of an excitation that results from quantum coherence allows the excitation to 'memorize' its earlier location. This is very different from the random hopping motion associated with classic mechanisms of energy transfer. Engel et al.8 have speculated that quantum coherence allows antennas to search for the lowest-energy state of the complex more efficiently than they could using classical mechanisms; this, in turn, might enhance the efficiency of energy transfer towards a reaction centre. It has also been argued11 recently that long-lived quantum coherence might help excitations to avoid local 'traps' (energy minima) that they encounter in the energy landscape on their way to a reaction centre.

But Collini et al.1 suggest that their algal antenna complexes are special. Unlike most photosynthetic pigments, the eight bilin pigments in each cryptophyte antenna are covalently bound to the proteins of the complex. The authors speculate that this covalent attachment helps prevent the loss of quantum coherence. This, in turn, would explain why the lifetime of quantum coherence at room temperature is so long in cryptophyte antennas. The researchers also propose that quantum coherence might 'wire' together the final energy acceptors in cryptophyte antennas, thus compensating for the relatively weak electronic couplings between the pigments in the complex.

Much work clearly remains to be done. For example, it would be interesting to establish quantitatively whether or not photosynthetic light harvesting that involves quantum coherence is truly more efficient than it would be using classical mechanisms of energy transfer alone. But for now, Collini et al. have shown that quantum coherence can't be ignored in the search for explanations of the remarkable efficiency of photosynthetic energy-transfer processes