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Sunlight absorbed by
bacteriochlorophyll (green) within the FMO protein (gray)
generates a wavelike motion of excitation energy whose quantum
mechanical properties can be mapped through the use of
two-dimensional electronic spectroscopy.
Image courtesy of Greg Engel,
Lawrence Berkeley National Laboratory, Physical Biosciences
Division |
"We have obtained the first direct evidence
that remarkably long-lived wavelike electronic quantum coherence plays
an important part in energy transfer processes during photosynthesis,"
said Graham Fleming, the principal investigator for the study. “This
wavelike characteristic can explain 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.”
Fleming is the Deputy Director of Berkeley Lab, a
professor of chemistry at UC Berkeley, and an internationally
acclaimed leader in spectroscopic studies of the photosynthetic
process. In a paper entitled, Evidence for wavelike energy transfer
through quantum coherence in photosynthetic systems, he and his
collaborators report the detection of “quantum beating” signals,
coherent electronic oscillations in both donor and acceptor molecules,
generated by light-induced energy excitations, like the ripples formed
when stones are tossed into a pond.
Electronic spectroscopy measurements made on a
femtosecond (millionths of a billionth of a second) time-scale showed
these oscillations meeting and interfering constructively, forming
wavelike motions of energy (superposition states) that can explore all
potential energy pathways simultaneously and reversibly, meaning they
can retreat from wrong pathways with no penalty. This finding
contradicts the classical description of the photosynthetic energy
transfer process as one in which excitation energy hops from
light-capturing pigment molecules to reaction center molecules
step-by-step down the molecular energy ladder.
"The classical hopping description of the energy
transfer process is both inadequate and inaccurate," said Fleming. "It
gives the wrong picture of how the process actually works, and misses
a crucial aspect of the reason for the wonderful efficiency."
Co-authoring the Nature paper with Fleming were
Gregory Engel, who was first author, Tessa Calhoun, Elizabeth Read,
Tae-Kyu Ahn, Tomas Mancal and Yuan-Chung Cheng, all of whom held joint
appointments with Berkeley Lab’s Physical Biosciences Division and the
UC Berkeley Chemistry Department at the time of the study, plus Robert
Blankenship, from the Washington University in St. Louis.
The photosynthetic technique for transferring
energy from one molecular system to another should make any short-list
of Mother Nature’s spectacular accomplishments. If we can learn enough
to emulate this process, we might be able to create artificial
versions of photosynthesis that would help us effectively tap into the
sun as a clean, efficient, sustainable and carbon-neutral source of
energy.
Towards this end, Fleming and his research group
have developed a technique called two-dimensional electronic
spectroscopy that enables them to follow the flow of light-induced
excitation energy through molecular complexes with femtosecond
temporal resolution. The technique involves sequentially flashing a
sample with femtosecond pulses of light from three laser beams. A
fourth beam is used as a local oscillator to amplify and detect the
resulting spectroscopic signals as the excitation energy from the
laser lights is transferred from one molecule to the next. (The
excitation energy changes the way each molecule absorbs and emits
light.)
Fleming has compared 2-D electronic spectroscopy to
the technique used in the early super-heterodyne radios, where an
incoming high frequency radio signal was converted by an oscillator to
a lower frequency for more controllable amplification and better
reception. In the case of 2-D electronic spectroscopy, scientists can
track the transfer of energy between molecules that are coupled (connected)
through their electronic and vibrational states in any photoactive
system, macromolecular assembly or nanostructure.
Fleming and his group first described 2-D
electronic spectroscopy in a 2005 Nature paper, when they used the
technique to observe electronic couplings in the Fenna-Matthews-Olson
(FMO) photosynthetic light-harvesting protein, a molecular complex in
green sulphur bacteria.
Said Engel, "The 2005 paper was the first
biological application of this technique, now we have used 2-D
electronic spectroscopy to discover a new phenomenon in photosynthetic
systems. While the possibility that photosynthetic energy transfer
might involve quantum oscillations was first suggested more than 70
years ago, the wavelike motion of excitation energy had never been
observed until now."
As in the 2005 paper, the FMO protein was again the
target. FMO 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.
"To observe the quantum beats, 2-D spectra were
taken at 33 population times, ranging from 0 to 660 femtoseconds,"
said Engel. "In these spectra, the lowest-energy exciton (a bound
electron-hole pair formed when an incoming photon boosts an electron
out of the valence energy band into the conduction band) gives rise to
a diagonal peak near 825 nanometers that clearly oscillates. The
associated cross-peak amplitude also appears to oscillate.
Surprisingly, this quantum beating lasted the entire 660 femtoseconds."
Engel said the duration of the quantum beating
signals was unexpected because the general scientific assumption had
been that the electronic coherences responsible for such oscillations
are rapidly destroyed.
"For this reason, the transfer of electronic
coherence between excitons during relaxation has usually been ignored,"
Engel said. "By demonstrating that the energy transfer process does
involve electronic coherence and that this coherence is much stronger
than we would ever have expected, we have shown that the process can
be much more efficient than the classical view could explain. However,
we still don’t know to what degree photosynthesis benefits from these
quantum effects."
Engel said one of the next steps for the Fleming
group in this line of research will be to look at the effects of
temperature changes on the photosynthetic energy transfer process. The
results for this latest paper in Nature were obtained from FMO
complexes kept at 77 Kelvin. The group will also be looking at broader
bandwidths of energy using different colors of light pulses to map out
everything that is going on, not just energy transfer. Ultimately, the
idea is to gain a much better understanding how Nature not only
transfers energy from one molecular system to another, but is also
able to convert it into useful forms.
"Nature has had about 2.7 billion years to perfect
photosynthesis, so there are huge lessons that remain for us to learn,”
Engel said. “The results we’re reporting in this latest paper, however,
at least give us a new way to think about the design of future
artificial photosynthesis systems." |
