Coherence Maps Reveal Photosynthesis Quantum Mechanics
Researchers have used coherence maps to shed light on how energy moves in a photosynthetic molecular complex. Their results show that disorder—what might seem like a bug for some biological systems—is actually a “feature” that allows efficient energy transfer to occur.
Inside their labs, scientists marvel at a strange state of matter known as exciton condensates. But now a University of Chicago study suggests that photosynthesis and exciton condensates aren’t as far apart as they look.
A mix of experiments and theory has helped to clarify how energy is transferred along a series of proteins that leads straight to the photosynthzing reaction center in a plant. But despite this clearer understanding, the process remains a puzzle under classical physics. For example, if these proteins were all arranged in a very regular fashion, with each protein positioned at an even distance from its neighbour, it would be very hard for photons to reach the centre of the complex without hitting the surrounding proteins.
Previous work had suggested that some of the light-sensitive molecules in these proteins could remain in two different states at the same time, a quantum effect known as vibrational coherence. But that was only a hint of the quantum weirdness that actually exists here. A new study by Makri’s group, using a technique called coherence maps, has unambiguously found that the excited-state vibronic coherence of these molecules does indeed play an important role in the efficient transport of energy in the FMO complex.
A photon is the particle of light that starts the energy transfer chain in photosynthetic reactions. The process that powers our world needs to be fine-tuned for every photon that passes through a molecule or two of chlorophyll, or one of the many other molecules involved in photosynthesis.
To study those molecule-level interactions, Coker and his colleagues use a technique called quantum spectroscopy. They pass white light through a sample and measure the signatures of all the different wavelengths it absorbs. Each molecule has a signature that looks like a dilapidated picket fence, except most of the slats are missing.
For years, physical chemists have wondered whether efficient energy transport could occur if the wavelike electronic excitations of chromophores—equivalent to the acoustic beats audible when sound waves of different frequencies interfere with each other—were somehow synchronized. But if that synchrony occurred, it would require an extremely precise arrangement of the molecule, and photosynthesis would be impossible.
It has long been suspected that the efficiency of energy transfer during photosynthesis results from synchronization between wavelike electronic excitations – known as excitons – in different chromophores. It is much like the beats that are audible when sound waves of a similar frequency interfere with each other. This synchronization – or coherence – is needed to avoid energy being lost in random “hopping” between the many possible pathways to the reaction center.
In the 1990s, advanced ultrafast spectroscopies, including two-dimensional electronic spectra (2D-ES), revealed long-lived vibrational coherences on the order of picoseconds in bacterial and plant light-harvesting complexes. These results, called coherence maps, allowed chemists to calculate the true quantum efficiency of these energy-transfer steps.
In 2007 physical chemist Graham Fleming, who studies the photosynthetic system with his Berkeley colleagues, proposed that the efficiency of energy transfer to the reaction center comes from the synchronization of wavelike electronic oscillations between pigment molecules – known as excitons. These signals are similar to acoustic beats, the interference pattern audible when sound waves of the same frequency interfere, and they enable excitation energy to sample many potential pathways to the reaction center before it is discarded by random hopping between chromophores.
Since then, advanced ultrafast techniques – such as two-dimensional electronic spectroscopy (2D-ES) – have demonstrated that coherent superpositions of vibrational and vibronic (mixed excitonic-vibrational) states in the FMO protein can persist for picoseconds. These results, combined with theoretical models, support the notion that quantum coherence enhances photosynthesis efficiency by reducing variations in excitation distributions between the antenna and reaction center.
The next step will be to test whether these coherences really do improve the efficiency of natural photosynthesis systems under physiological conditions. Using an accelerated version of dephasing, scientists will compare the behavior of the photosynthetic complexes when dephasing rates are optimized with those under normal physiological conditions.