REVIEW
◥PHOTOSYNTHESIS
Light harvesting in oxygenic photosynthesis:
Structural biology meets spectroscopy
Roberta Croce^1 *and Herbert van Amerongen^2
Oxygenic photosynthesis is the main process that drives life on earth. It starts with the harvesting of solar
photons that, after transformation into electronic excitations, lead to charge separation in the reaction
centers of photosystems I and II (PSI and PSII). These photosystems are large, modular pigment-protein
complexes that work in series to fuel the formation of carbohydrates, concomitantly producing molecular
oxygen. Recent advances in cryo–electron microscopy have enabled the determination of PSI and PSII
structures in complex with light-harvesting components called“supercomplexes”from different
organisms at near-atomic resolution. Here, we review the structural and spectroscopic aspects of PSI and
PSII from plants and algae that directly relate to their light-harvesting properties, with special attention
paid to the pathways and efficiency of excitation energy transfer and the regulatory aspects.
P
rimary production on our planet is per-
formed by the process of photosynthe-
sis ( 1 ). The mechanisms through which
living organisms convert light energy into
chemical energy are complicated and
diverse. Although a number of subprocesses
have been studied at considerable depth, there
are still many knowledge gaps concerning the
overall performance. Understanding oxygenic
photosynthesis in particular is essential for
improving photosynthetic efficiency to increase
crop productivity ( 2 , 3 ). Recent proofs of prin-
ciple showed that subprocesses in both the
light and dark phase of photosynthesis can be
improved, leading to a substantial increase of
biomass production ( 4 – 7 ). These advances
canonlybemadebybuildingonavastamount
of fundamental research performed in numer-
ous laboratories around the world.
Photosynthesis research has addressed many
detailed aspects of the performance of specific
subunits, whereas the interaction between sub-
units remained underexposed. Progress is now
being made on understanding higher-level
organizations of components with the publication
of the structures of a variety of photosynthetic
multiprotein complexes (“supercomplexes”)at
near-atomic resolution. With these structures,
we can now see in detail how the subcom-
plexes are physically connected to each other,
which will contribute to our understanding
of how they functionally interact. Complexes
from a variety of organisms are also becoming
available, informing on the diversity of mech-
anisms. The central core of these complexes
is common to all organisms, whereas other
features show variations related to adaptation
to different environmental conditions. In
this review, we discuss a number of recently
determined structures of supercomplexes of
photosystems I and II (PSI and PSII), the main
players in the light phase of oxygenic photo-
synthesis. Together, they capture sunlight to
extract electrons from water (PSII) and reduce
NADP+to NADPH (PSI), whereas in parallel,
they contribute to the creation of a proton
gradient used for ATP formation. NADPH and
ATP are then used in the dark reactions to
synthesize carbohydrates from CO 2 in the
Calvin-Benson-Bassham cycle. Here, we ana-
lyze how these structures relate to earlier spec-
troscopic and functional studies and arrive at
some unexpected outcomes that should be
further addressed in future research.The photosystems
The basic working principles of the PSI and
PSII supercomplexes are the same: Light is
harvested by their associated pigments (chlo-
rophylls and carotenoids; Box 1 and Fig. 1) and
the resulting excitation energy is transferred,
mainly through closely spaced chlorophylla(Chla) molecules, to the reaction center (RC)
complex, where a stable charge separation (CS)
is created ( 8 ).
A typical plant photosystem contains ~150
Chls per RC, meaning that it can absorb at
most one photon every millisecond ( 1 ). After
light absorption has occurred, the energy is
stored in the excited state of the pigments for
a very short amount of time [for chlorophylls
in the thylakoid membrane, the excited-state
lifetime (t)istypically2ns( 9 )] as all molecules
relax rapidly to the ground state through a
number of deexcitation processes. To ensure a
high photon-to-electron conversion efficiency
(also called quantum efficiency), it is therefore
necessary that the harvested energy is transferred
to the RC fast enough to beat the other de-
excitation processes. The time that it takes for
an excitation to reach the RC and induce CS
(tCS) varies considerably, from ~20 ps in the
PSI core ( 10 , 11 )to~300psinlargePSIIcom-
plexes ( 12 , 13 ). For the PSI core, this leads to a
maximum quantum efficiency of CS ofφCS=
1 – tCS(20 ps)/t(2 ns) = 0.99, whereas it can be
φCS=1–tCS(300 ps)/t(2 ns) = 0.85 for PSII in
vivo. However, in most conditions, and espe-
cially in high light when photoprotective mech-
anisms are turned on, the quantum efficiency
can decrease substantially ( 4 ). It is important
to realize that this quantum efficiency is not
the same as the photosynthetic efficiency, which
compares the energy of the final products
(sugars) with the original energy contained in
the absorbed photons and depends on many
additional processes [see, e.g., ( 2 )and( 14 )].
Both PSI and PSII can be divided into two
parts: (i) a core complex, which contains both
the RC and the inner antenna system, coordi-
nating ~100 Chlsain PSI and ~35 Chlsain
PSII, and is highly conserved in cyanobacteria,
algae, and plants; and (ii) an outer antenna,
the size and composition of which depend on
the type of organism and growth conditions
( 15 , 16 ). The antenna is needed to increase the
absorption cross section of the RC because even
in the highest possible natural light conditions,
one Chl would absorb a photon only ~10 timesRESEARCH
Croceet al.,Science 369 , eaay2058 (2020) 21 August 2020 1of9
(^1) Department of Physics and Astronomy, Faculty of Science,
Vrije Universiteit Amsterdam, Amsterdam, Netherlands.
(^2) Laboratory of Biophysics, Wageningen University &
Research, Wageningen, Netherlands.
*Corresponding author. Email: [email protected]
Box 1. Pigments and EET between them (see Fig. 1).
Plants and green algae make exclusive use of Chlsaandb, whereas some algae contain Chlc( 23 )
and some cyanobacteria can synthesize Chldand Chlf( 102 , 103 ). Directly after excitation of a Chl,
relaxation (internal conversion) takes place within at most several hundred femtoseconds to the first
excited state, from where EET to neighboring Chls takes place. The rate of transfer (k) can be
approximated by making use of Förster theory ( 104 ) [for the equation, see Fig. 1; numbers were taken
from ( 105 )]. Even for the short distances present in LHCs, this theory provides reasonable values for
amplitudes and rates of transfer ( 45 , 105 ). After rapid thermal equilibration of an excitation within a Chl
a–Chlbpair as indicated in Fig. 1, the probability of finding the excitation on Chlaandbat room
temperature is 0.90 and 0.10, respectively, using either the principle of detailed balance or applying the
Boltzmann equilibrium equation. In addition, carotenoids are present in photosynthetic organisms and
are involved in both light harvesting and photoprotection. Carotenoids absorb green and blue light and
rapidly (<1 ps) transfer their energy to neighboring Chls ( 106 ).