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Principles of light harvesting from single

photosynthetic complexes
rsfs.royalsocietypublishing.org

G. S. Schlau-Cohen
Department of Chemistry, Massachusetts Institute of Technology, 77 Massachusetts Avenue, 6-225,
Cambridge, MA 02139, USA

Review
Cite this article: Schlau-Cohen GS. 2015
Principles of light harvesting from single
photosynthetic complexes. Interface Focus 5:
20140088.
http://dx.doi.org/10.1098/rsfs.2014.0088
One contribution of 11 to a theme issue Do
we need a global project on artificial photosynthesis (solar fuels and chemicals)?.
Subject Areas:
biochemistry, biophysics, chemical physics
Keywords:
light harvesting, photosynthesis,
single molecule spectroscopy
Author for correspondence:
G. S. Schlau-Cohen
e-mail: gssc@mit.edu

Photosynthetic systems harness sunlight to power most life on Earth. In the

initial steps of photosynthetic light harvesting, absorbed energy is converted
to chemical energy with near-unity quantum efficiency. This is achieved by
an efficient, directional and regulated flow of energy through a network of
proteins. Here, we discuss the following three key principles of this flow and
of photosynthetic light harvesting: thermal fluctuations of the protein structure; intrinsic conformational switches with defined functional consequences;
and environmentally triggered conformational switches. Through these
principles, photosynthetic systems balance two types of operational costs:
metabolic costs, or the cost of maintaining and running the molecular machinery, and opportunity costs, or the cost of losing any operational time.
Understanding how the molecular machinery and dynamics are designed to
balance these costs may provide a blueprint for improved artificial lightharvesting devices. With a multi-disciplinary approach combining knowledge
of biology, this blueprint could lead to low-cost and more effective solar energy
conversion. Photosynthetic systems achieve widespread light harvesting across
the Earths surface; in the face of our growing energy needs, this is functionality
we need to replicate, and perhaps emulate.

1. Introduction
Sunlight is a ubiquitous and abundant energy source. In just 1 h, enough energy
hits the Earths surface (approx. 4.320 J) to provide for human consumption over
an entire year (approx. 4.120 J) [1]. The challenge lies in efficiently capturing and
storing this energy. Photosynthetic organisms have met this challenge, and are
able to use sunlight to fuel almost all life on Earth [2]. The molecular machinery
behind this large-scale power conversion process can serve as a guide for the
development of solar energy sources [36]. The efforts towards artificial photosynthesis can be considered in three categories: (i) create elements inspired by
photosynthetic systems [711]; (ii) incorporate components from photosynthetic
organisms [1215]; and (iii) use living organisms, either wild-type or genetically
modified [1619]. Recent work upregulating light harvesting through downstream processes has been particularly promising. The workflow behind all
of these efforts is summarized in figure 1. Essentially, realization of a sustainable
solar energy device requires that we understand the mechanisms of photosynthesis, use these mechanisms to develop smarter designs and with these
designs build optimized devices. Finally, advocating for the widespread usage
of these devices is an equally critical component. We focus on the first step of
this process: understanding natural photosynthesis. To allow this understanding
to be useful for later steps, we highlight general principles observed in photosynthetic light harvesting, which may be implemented in artificial systems
dramatically different from the natural systems.
Several aspects of photosynthesis exhibit functionality that far exceeds what
we can currently replicate in devices. Although overall power conversion efficiency is, at best, only 7% [20], in the early events in photosynthesis, absorbed
sunlight is converted to electricity with near-unity quantum efficiency [2,20].
This electricity is part of generating the transmembrane electrochemical potential
that drives photosynthesis. This remarkable efficiency is achieved by a series of
energy transfer steps through a network of pigmentprotein complexes (PPCs),

& 2015 The Author(s) Published by the Royal Society. All rights reserved.

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understand
photosynthesis

smarter
design

optimized
devices

widespread
usage

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Figure 1. Flow chart shows the pathway to artificial photosynthesis. The first
step is understanding photosynthesis, which can lead to a smarter design,
which, in turn, can give rise to optimized devices. Finally, the performance
of optimized devices can be leveraged for widespread usage.

Figure 2. Schematic of photosystem II, one of the light-harvesting super-complexes from higher plants. Antenna complexes surround the core complexes and
the reaction centre. Absorbed sunlight transfers rapidly, efficiently and directionally to reach the reaction centre, where charge separation occurs. (Adapted from
[4].) (Online version in colour.)

2. Robust to disorder
At room temperature, protein structures are not static, but
instead fluctuate owing to thermal motion. In PPCs, the pigments are densely packed within the protein matrix [23,24].
This produces relatively strong electrodynamic couplings
between the pigments and between the pigments and the surrounding protein that control the excited state energies and
dynamics. The strength of these couplings is highly sensitive
to intermolecular distances [25,26]. This leads to the following question: how do photosynthetic systems maintain
near-unity quantum efficiency in the face of structural fluctuations? In other words, how are the excited state properties
simultaneously sensitive to structure and robust to the
thermal motion of the structure?
Single-molecule fluorescence spectroscopy reports on the
excited states of individual proteins, and thus determines
the distribution that results from thermal fluctuations.
The anti-Brownian electrokinetic (ABEL) trap is a singlemolecule technique that enables studies of single proteins in
a solution-phase (non-perturbative) environment, accessing
the intrinsic behaviour [27,28]. By simultaneous measurements of fluorescence intensity, lifetime and spectrum,
the excited state properties of individual photosynthetic proteins can be characterized [29] without perturbation from
the surface attachment or encapsulation used in previous
studies [30,31].
The antenna complex from purple bacteria is light-harvesting complex 2 (LH2), shown in figure 3a. LH2 is a nonameric
assembly of protein subunits. Each subunit contains three bacteriochlorophyll (BChl), which form two concentric rings, and
one carotenoid surrounded by a protein matrix. Previous experiments have characterized the excited state dynamics [33].
Energy rapidly transfers (in less than 1 ps) to the lower energy
ring, and fluorescence occurs out of this ring. LH2 has
an order of magnitude more inhomogeneity in excited state
energies than other bacterial LHCs, suggesting that it is particularly sensitive to thermal fluctuations [33]. Specifically,
LH2 has an inhomogeneous broadening of 300 cm21 [34],

Interface Focus 5: 20140088

as shown in figure 2. PPCs are carotenoids and chlorophylls

surrounded by a protein matrix. Energy migrates hundreds of
nanometres through this network to reach the reaction centre
(RC), where the energy drives an electron transfer chain,
which, in turn, drives downstream biochemistry [2,21]. How
photosynthetic systems achieve an efficient and directional
energy flow remains incompletely understood.
In most systems, the majority of PPCs are the antenna complexes, which absorb sunlight and perform the initial energy
transfer steps. While the antenna complexes differ in structural
motif across organisms, the RC structures are conserved [4]. The
RCs are metabolically expensive to construct, as they must
complete a complex electron transfer chain [2]. The antenna
complexes lack electron transfer functionality, but ensure the
electron flux is optimal. That is, water-splitting requires four
electrons, and all four electrons must arrive before the intermediates relax. At the same time, electrons arriving faster
than the speed of the water-splitting reaction cannot be used,
and may generate deleterious products. These two limits
mean that the rate of charge generation must be regulated.
The antenna complexes are responsible for this regulation,
and implement multiple multi-time-scale processes that prevent the build-up of excess energy. These processes can
obfuscate the intrinsic characteristics of the antenna complexes
as well as the mechanisms of the individual processes.
Only through understanding the behaviour and dynamics
of PPCs, however, can we understand how photosynthetic
systems achieve high quantum efficiency in conversion of
absorbed sunlight to electricity, and how this efficiency responds
to the orders of magnitude changes in solar flux seen in nature.
In studying the response to these changes in solar flux, one constraint that emerges is the balance of two types of costs: metabolic
cost and opportunity cost. Metabolic cost is the energy spent
to construct and repair and insert the molecular machinery.
Opportunity cost is not capturing energy owing to inoperability
or non-optimal functioning of the molecular machinery [22].
Optimizing these two costs guides the principles behind light
harvesting under natural conditions.
Here, we describe three key principles by which natural
photosynthesis achieves efficient and effective light-harvesting
functionality. The identification of these principles can aid the
development of solar energy devices. We focus on phenomena
observed by studying single antenna complexes. For the first
principle, we explore how these systems are robust to fluctuations in the protein structure owing to thermal motion. We
characterize the resultant energetic disorder by experimentally
characterizing the distribution of behaviours. For the
second principle, we discuss how discrete conformational
switches allow one protein to perform multiple functions. For
the third principle, we examine how the cellular environment
can be a trigger for such conformational changes, and how
this enables the protein to participate in a system-wide feedback loop. We conclude this perspective with a discussion of
how these principles can be applied to the design of an artificial
photosynthetic device.

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(c)

12.5

45

1
*

10
time (s)

4
time (s)

Interface Focus 5: 20140088

(d)

15

(e)
8
lifetime (ns)

1.5

0.5

0
850
900
wavelength (nm)

950

15
intensity (cpms)

30

Figure 3. Single-molecule data of light-harvesting complex 2 (LH2) from purple bacteria. (a) The structural model from X-ray crystallography of LH2 [23]. The BChl
are shown in red, the carotenoids in blue and the protein matrix in yellow. Two representative intensity lifetime traces of single LH2 complexes are shown in
(b,c) for excitation into the B800 band of BChl. The spectra that correspond to two of the intensity levels in (b) are shown in (d ). The spectra reveal that the intensity
change at 11 s in (b) is accompanied by not just a lifetime but also a spectral change. This arises from thermal fluctuations. (e) By plotting the distribution of
intensity levels with their concomitant lifetimes on a two-dimensional scatter plot, three states are revealed. These states are labelled A, B and C. (Modified from
[32].) (Online version in colour.)

whereas another widely studied photosynthetic complex, the

FennaMatthewsOlson complex, has an inhomogeneous
broadening of just 35 cm21 [35]. To investigate the intrinsic inhomogeneity, we apply the ABEL trap to study single
LH2 complexes.
By simultaneously recording fluorescence intensity,
lifetime and spectra, changes in the excited state manifold
can be explored. Intensity and lifetime traces of two representative complexes are shown in figure 3b,c. The corresponding
fluorescence spectra for the shaded intensity levels in
figure 3b are displayed in figure 3d. As illustrated here,
occasionally (approx. 5%) the intensity changes were
accompanied by a spectral change, in this case a 5 nm red
shift. By examining thousands of individual complexes, the
intensity/lifetime changes and spectral changes were found
to be uncorrelated. Furthermore, the spectral changes were
small; the spectra shifted 5 nm or less. At these wavelengths,
a 5 nm shift corresponds to a small amount of energy,
only approximately 1/2kT [32]. Thus, the shifts induced by
thermal fluctuations are not large enough to create either a
barrier (shift to higher energy) or a trap (shift to lower
energy), and so the spectral dynamics observed will not
interfere with the energy transfer dynamics.
Overall, to be robust to the disorder from thermal fluctuations, the protein functions so that the fluctuations produce
energy shifts ,kT. With this constraint, photosynthetic systems balance both metabolic and opportunity costs: they do
not pay the metabolic cost to construct a rigid system without
fluctuations, e.g. by inserting multiple bonds or strong electrostatic interactions into the protein, nor do they pay the
opportunity cost of lost light harvesting from fluctuations
interrupting the energy transport chain.

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25.0

90

counts/103

lifetime (ns)

(b)

intensity (cpms)

(a)

3. Multi-functionality through conformational

switches
As shown in the traces in figure 3b,c, intensity and lifetime
primarily exhibit correlated changes. Similar intensities
occasionally will have very different concomitant lifetimes,
however, indicated with an asterisk in figure 3c. To investigate the correlations between intensity and lifetime, each
period of constant intensity with its concomitant lifetime is
represented with a dot on the two-dimensional intensity lifetime scatter plot shown in figure 3e. The dots form three
clusters as determined by a Gaussian mixture model,
shown with rainbow lines. These three clusters are labelled
as states A, B and C.
These results demonstrate that states A and B arise from a
photoactivated, reversible quenching process [32]. As illustrated by the direct proportionality between states A and B,
state B exhibits an increased rate of quenching, or nonradiative decay off the emissive state. Non-radiative decay
occurs through the electronic excitation dissipating into the
vibrations on the pigment, which, in turn, transfer to the
vibrations in the protein. A conformational change could produce a conformation that facilitates this process through
increased coupling between the electronically excited state
and the pigment vibrations or between the vibrations on the
pigment and the vibrations on the protein. Thus, state B is
most likely to be formed through a conformational change [32].
A conformational change is also supported by the changes
in the relative populations of states A and B with excitation fluence. The rate of transition from state A to state B increases
roughly linearly with excitation fluence, indicating a photoactivated process [32]. Each photon deposits enough energy

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(a)

(b)

frequency

30

60

0
time (s)

30

60

2.5
intensity (cpms)

5.0

into the protein to enable a conformational change, which

causes the probability of the transition to increase with the
number of photons [36]. In contrast, the rate of transition
from state B to state A is independent of excitation fluence, indicating a thermal process [32]. State C, however, most likely
arises from an irreversible photodegradation process [32].
The two conformations of states A and B, and their
dynamics allow a single protein to have both light-harvesting
and photoprotective functionality. Under high light intensities,
many LH2 complexes switch into a quenched state via a conformational switch, where they can safely dissipate excess
energy. Under low light intensities, most LH2 complexes
revert into the unquenched state via thermal fluctuations.
Instead of assigning a single function to a single protein,
here, we observe that photosynthetic organisms embed multifunctionality into LH2. In this way, they control the metabolic
cost associated with protein synthesis.

4. Environmentally controlled functionality

In addition to the intrinsic conformational heterogeneity and
photo-induced conformational dynamics discussed in 3,
photosynthetic proteins can also exhibit conformational
dynamics in response to changes in the cellular environment
caused by fluctuations in light intensity [22]. In particular,
these environmentally induced conformational dynamics
have been observed and explored in higher plants, and so, in
this section, we focus on these type of dynamics in green
plants. Under low light conditions, such as a cloudy day, all
absorbed sunlight is converted to electricity for photosynthesis
[20]. Under high light conditions, such as direct sunlight, the
capacity of the antenna complexes to absorb and transfer
energy exceeds the capacity of downstream photosynthesis.
To prevent a build-up of excess energy, plants and algae dissipate this energy through a series of multi-time-scale processes.
These processes are collectively known as non-photochemical
quenching (NPQ) [37]. The short-time, energy-dependent component of NPQ is qE, and is triggered by a pH drop in the
lumen and the resulting electrochemical gradient across the
membrane [37,38]. While many of the time scales of NPQ
have been identified, the mechanism and specific PPC responsible for quenching remains under debate. Specifically, which
PPC, which carotenoid, and whether or not charge transfer
states play a role have all been discussed [3739].
One known effect of the drop in lumen pH is to cause PsbS,
a non-pigment binding photosynthetic protein, to activate
quenching [40]. In this way, the environmental conditions

control whether PsbS is inactive or active. Thus, the change

here is not isolated to a single protein, as discussed in 3, but
rather is part of a larger feedback loop within the organism
[22]. An area of active investigation is the impact of the environmental conditions associated with high light on the primary
antenna complex from green plants, light-harvesting complex
II (LHCII). LHCII is trimeric, and each monomer contains 14
chlorophyll (Chl), six Chl-b and eight Chl-a, and four carotenoids surrounded by a protein matrix [24]. Energy rapidly
transfers to the Chl-a, and fluorescence occurs out of the
Chl-a band [4147]. On-going efforts are focused on characterizing the changes in the excited state manifold of LHCII
under conditions that mimic high light. The questions are
whether LHCII is the site of dissipation, and, if so, what the
photophysical mechanism of dissipation is.
Figure 4 shows the behaviours of single LHCII complexes.
Two intensity traces of single LHCII complexes are shown in
figure 4a. These traces exhibit representative dynamics. The
intensity changes from the higher (dominant) level to a lower
level, and vice versa (figure 4a, right). The individual complexes also transiently enter into and recover from a dark
state in a process known as blinking, observed in the brief disappearance of fluorescence (e.g. event at 35 s in figure 4a, left).
Assuming a constant absorbance, the fluorescence decrease
indicates a quenching process is occurring in both the lowintensity complexes and the ones in a dark state. To investigate
the distribution of intensity levels, we construct a histogram
from all periods of constant intensity as determined by a
change-point-finding algorithm (figure 4b). The histogram
shows significant population in both the higher intensity and
lower intensity levels, revealing a significant population of
LHCII is in a quenched conformation. The correlation of this
quenched conformation with conditions that mimic high
light is currently under investigation. Previous experiments
have extensively studied the correlation between the dark
states and conditions that mimic high light. In this work, blinking was shown to correlate with these conditions, leading to the
hypothesis that blinking underlies qE [48]. Additionally, experiments suggest the underlying mechanism may be dissipation
on the carotenoids by increased coupling between the Chl and
the carotenoids [49,50] or charge transfer [51,52].
While the detailed molecular mechanisms require further
experimentation, it can be argued that NPQ serves as a feedback
loop to optimize between metabolic cost and opportunity
cost. In this way, systems are able to protect their expensive molecular machinery, while keeping the input, the photoenergy, as
close to the capacity of downstream photosynthesis as possible.
One process by which this feedback loop is implemented is

Interface Focus 5: 20140088

Figure 4. Single-molecule data from light-harvesting complex II (LHCII) from green plants. (a) Two representative intensity traces of single LHCII complexes. Single
complexes switch between intensity levels. (b) A histogram of the intensity levels reveals higher intensity and lower intensity states. (Online version in colour.)

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intensity (cpms)

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5. Application to artificial devices

Acknowledgements. The author acknowledges past and present collaborators on this work: W.E. Moerner, Hsiang-Yu Yang, Richard Cogdell,
Quan Wang, June Southall, Roberta Croce, Rienk van Grondelle,
Tjaart Kruger, Michal Gwizdala and Pengqi Xu.
Funding statement. This material is based on work supported in part by
the U.S. Department of Energy, Office of Science, Office of Basic
Energy Sciences, Division of Chemical Sciences, Geosciences, and
Biosciences under award no. DE-FG0207ER15892 (to W.E.M.). The
author also acknowledges a Postdoctoral Fellowship from the Center
for Molecular Analysis and Design at Stanford University. The
author would like to acknowledge the Royal Society for travel support.

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Photosynthesis generates enough energy from sunlight to

power most life on Earth. Thus, it provides a natural source
of inspiration for improving the design of artificial solar
energy devices. There are several principles of the biological
circuitry that could improve these devices. Here, we have
highlighted three of these principles: we have discussed
how photosynthetic proteins are robust to disorder; exhibit
multi-functionality through conformational switches; and
have environmentally controlled functionality.
One overarching tenet that emerges from studying biological systems is that biological structures are dynamic. They are
constantly fluctuating and responding to the organisms changing needs. Often, artificial devices are designed as static
structures that are either operational or broken. However, biological systems exploit their intrinsic lack of rigidity to embed
additional functionality in thermal fluctuations and multiple
conformations. In this way, they are able to balance metabolic
cost and opportunity cost under the varying environmental
conditions found in nature. Current research focusing on building bioinspired devices has achieved impressive initial results.
Photosynthetic systems have evolved over billions of years to
balance metabolic and opportunity costs by dynamically
adapting to the local environment heterogeneity and dynamic
structures. This behaviour could be replicated in artificial systems by switching the device from one mode to another,

such as through a chemical transition [10], or selectively

using concentrators to control the amount of incident sunlight.
Additionally, the observation of dynamic and static heterogeneity suggests that natural systems do not require perfect
structural and functional precision, and this type of flexibility
could be advantageous in the design and manufacture of
cost-effective devices.
By incorporating the dynamic behaviours observed in
nature, the performance of artificial devices could be
improved to meet our increasingly critical energy needs.
With these steps, we move down the steps illustrated in
figure 1. However, this is a fundamentally interdisciplinary
effort, requiring expertise in biology, material science
and engineering. As a result, success requires greater interdisciplinary communication and cooperation. This could be
initiated through efforts such as an exchange between natural
and artificial photosynthetic researchers, and sustained
through funding projects requiring multi-disciplinary teams.
The studies of biological dynamics described here are one
piece of the process of understanding and developing new
approaches to solar energy conversion.

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through protein conformational changes in response to changes

in the local environment, illustrating the ability of biological
systems to design feedback loops that extend throughout
the organism.

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