At the quantum level, plants are no longer plants. They are physics laboratories.

An artificial version of photosynthesis, the process by which green plants convert solar energy into electrochemical energy, would provide humanity with a clean and renewable source of electrical power. An artificial version of photosynthesis also would help scrub the atmosphere of excessive carbon dioxide that results from the burning of fossil fuels.

To reach this promised land, however, scientists need a far better understanding of how nature is able to transfer nearly 100 percent of the photons absorbed by the leaves of green plants to reaction centers for conversion into electrochemical energy. It has long been recognized that the key to this remarkable efficiency is speed—the transfer of the solar energy takes place almost instantaneously, so little energy is wasted as heat. But how this near-instantaneous energy transfer is accomplished had been a long-standing mystery, before a research effort led by Graham Fleming, a physical chemist with the Lawrence Berkeley National Laboratory (Berkeley Lab), in Berkeley, California.

With the development of a laser-based technique the team developed, called two-dimensional electronic spectroscopy, Fleming and his group have been able to track the flow of light-induced excitation energy through photosynthetic molecular complexes with femtosecond resolution. In the time it takes to pronounce the word femtosecond, a quadrillion femtoseconds have passed. They discovered that the secret behind the efficiency of photosynthetic energy transfer is quantum mechanics.

Prior to the discovery by Fleming and his group, photosynthetic energy transfer was described as a classical physical chemistry process in which light-induced excitation energy hops from light-capturing pigment molecules to reaction center molecules step-by-step down the molecular energy ladder. Fleming characterized this classical hopping description as both inadequate and inaccurate.

“We obtained the first direct evidence that remarkably long-lived wavelike electronic quantum coherence plays an important part in energy transfer processes during photosynthesis,” he said. “This wavelike characteristic explains the extreme efficiency of the energy transfer because it enables the system to simultaneously sample all the potential energy pathways and choose the most efficient one.”

The team reported that instead of excitation occupying one energy state at a time, the photosynthetic system performs a single quantum computation, sensing multiple different states all at once, selecting the correct answer and sending excitation energy back and forth throughout the system without penalty for reversing direction.

In 1932, French physicist Francis Perrin first proposed the possibility that quantum oscillations played a part in the transfer of energy. But as Gregory Engel, a former member of Fleming’s group and lead author on a paper published in the journal Nature that first reported this work in 2007, explained, “The wavelike motion of excitation energy had never been observed until our study.”

Light excites electrons in pigment molecules called chromophores—for plants, the main chromophore is chlorophyll. After moving through the chromophores the energy is trapped in a reaction center where it is used to produce carbohydrates.

“In natural light–harvesting systems, chlorophyll pigments are arranged together in an ‘antenna,’ sometimes with elegant symmetry and sometimes with apparent randomness, but always with a precise structure that is supplied by a protein scaffold,” wrote chemist Roseanne J. Sension of the University of Michigan in a commentary for Nature about the paper by Fleming and his group.

In addition to Fleming and Engel, the original discovery team included Tessa Calhoun, Elizabeth Read, Tae-Kyu Ahn, Tomáš Manˇcal, Yuan-Chung Cheng and Robert Blankenship. For this work, they targeted the Fenna-Matthews-Olson (FMO) antenna complex, a bacteriochlorophyll protein structure that is considered a model system for studying photosynthetic energy transfer because it consists of only seven pigment molecules and its chemistry has been well characterized. They used laser beams to flash on the antenna and record the effect in 2-D spectra at a temperature of 77 kelvin. Their results showed quantum beating signals that lasted as long as 660 femtoseconds, the maximum range tested.

This “long-lived” electronic quantum coherence came with a peak in the spectra at 825 nm that “clearly oscillates,” the team reported. “Its amplitude grows, fades and subsequently grows again. The peak’s shape evolves with these oscillations, becoming more elongated when weaker and rounder when the signal amplitude intensifies. The associated crosspeak amplitude also appears to oscillate.” That the oscillations lasted as long as 660 femtoseconds came as a surprise. “Our observation contrasted with the general assumption that the coherences responsible for such oscillations are destroyed very rapidly,” Engel explained.

In her commentary, Sension said, “The data also suggest that the protein scaffold might itself be structured to dampen fluctuations that would induce decoherence of the electronic excitation.” She called the observation of electronic coherences in such a complex system “remarkable,” despite the low temperature conditions under which the team acquired the data. “Assuming that the effect is general—that similar coherences occur in many different natural light–harvesting systems, and are observed at noncryogenic temperatures—we may find that nature, through its evolutionary algorithm, has settled on an inherently quantum-mechanical process for the critical mechanism of efficient light harvesting. This is an interesting lesson to be considered when designing artificial systems for this purpose.”

In commenting about the impact of this work on the development of artificial photosynthesis, Engel said, “Nature has had about 2.7 billion years to perfect photosynthesis, so there are huge lessons that remain for us to learn. Our results provided a new way to think about the design of
future artificial photosynthesis systems.”