Evidence that photosynthesis efficiency is based on quantum mechanics

January 17, 2014
leaves

Clover leaf (credit: Scott Robinson/Flickr)

Light-gathering macromolecules in plant cells transfer energy by taking advantage of molecular vibrations whose physical descriptions have no equivalents in classical physics, according to the first unambiguous theoretical evidence of quantum effects in photosynthesis, published in the journal Nature Communications (open access).

The majority of light-gathering macromolecules are composed of chromophores (responsible for the color of molecules) attached to proteins, which carry out the first step of photosynthesis, capturing sunlight and transferring the associated energy highly efficiently.

Previous experiments have suggested that energy is transferred in a wave-like manner, exploiting quantum phenomena, but crucially, a non-classical (quantum) explanation could not be conclusively proved because the phenomena identified could equally be described using classical physics.

Often, to observe or exploit quantum mechanical phenomena, systems need to be cooled to very low temperatures. This however does not seem to be the case in some biological systems, which display quantum properties even at ambient temperatures.

Now, University College London (UCL) scientists have attempted to identify features in these biological systems that can only be predicted by quantum physics, and for which no classical equivalents exist.

“Energy transfer in light-harvesting macromolecules is assisted by specific vibrational motions of the chromophores,” said Alexandra Olaya-Castro (UCL Physics & Astronomy), supervisor and co-author of the research. “We found that the properties of some of the chromophore vibrations that assist energy transfer during photosynthesis can never be described with classical laws, and moreover, this non-classical behavior enhances the efficiency of the energy transfer.”

Molecular vibrations are periodic motions of the atoms in a molecule, like the motion of a mass attached to a spring.  When the energy of a collective vibration of two chromphores matches the energy difference between the electronic transitions of these chromophores, a resonance occurs and efficient energy exchange between electronic and vibrational degrees of freedom takes place.

If the energy associated with the vibration is higher than the temperature scale, only a discrete unit or quantum of energy is exchanged. So as energy is transferred from one chromophore to the other, the collective vibration displays properties that have no classical counterpart.

The UCL team found the unambiguous signature of non-classicality is given by a negative joint probability of finding the chromophores with certain relative positions and momenta. In classical physics, probability distributions are always positive, meaning that they can be predicted.

“The negative values in these probability distributions are a manifestation of a truly quantum feature, that is, the coherent exchange of a single quantum of energy,” explained Edward O’Reilly (UCL Physics & Astronomy), first author of the study. “When this happens, electronic and vibrational degrees of freedom are jointly and transiently in a superposition of quantum states, a feature that can never be predicted with classical physics.”

Other biomolecular processes such as the transfer of electrons within macromolecules (as in reaction centers in photosynthetic systems), the structural change of a chromophore upon absorption of photons (as in vision processes) or the recognition of a molecule by another (as in olfaction processes), are also influenced by specific vibrational motions. The results of this research therefore suggest that a closer examination of the vibrational dynamics involved in these processes could provide other biological prototypes exploiting truly non-classical phenomena.

The finding of quantum effects in photosynthesis at ambient (room) temperatures also lends support for the “ORCH OR” theory proposed by Roger Penrose and Stuart Hameroff, which suggests that consciousness is based on quantum phenomena in microtubules.


Abstract of Nature Communications paper

Advancing the debate on quantum effects in light-initiated reactions in biology requires clear identification of non-classical features that these processes can exhibit and utilize. Here we show that in prototype dimers present in a variety of photosynthetic antennae, efficient vibration-assisted energy transfer in the sub-picosecond timescale and at room temperature can manifest and benefit from non-classical fluctuations of collective pigment motions. Non-classicality of initially thermalized vibrations is induced via coherent exciton–vibration interactions and is unambiguously indicated by negativities in the phase–space quasi-probability distribution of the effective collective mode coupled to the electronic dynamics. These quantum effects can be prompted upon incoherent input of excitation. Our results therefore suggest that investigation of the non-classical properties of vibrational motions assisting excitation and charge transport, photoreception and chemical sensing processes could be a touchstone for revealing a role for non-trivial quantum phenomena in biology.