Science - USA (2020-08-21)

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PHOTOSYNTHESIS


Light harvesting in oxygenic photosynthesis:


Structural biology meets spectroscopy


Roberta Croce*and Herbert van Amerongen


BACKGROUND:The harvesting of photons is
the first step in photosynthesis, the biological
process that transforms solar energy into chem-
ical energy. The photosynthetic membranes
of algae and plants are packed with protein
complexes binding many chlorophyll and
carotenoid pigments, which are combined to
form functional units. These units, called the
photosystem I and II (PSI and PSII) super-
complexes, are composedofareactioncenter
(RC) where photochemistry occurs and an
antenna comprising hundreds of pigments.
Because even direct sunlight is a dilute form of


energy, the antenna is crucial to increasing the
light-harvesting capacity of the RC. After light
is absorbed by a pigment in one of these com-
plexes, excitation energy transfer (EET) to a
nearby pigment occurs. EET proceeds until
the excitation reaches the RC, where charge
separation (CS) takes place. The faster the
energy reaches the RC, the higher the photon-
to-electron conversion efficiency is because
this process needs to beat the natural excited-
state decay of the pigments. The trapping in the


RCs of PSI and PSII in vivo occurs within 20 to
300 ps, and the maximal quantum efficiency is
close to 1.0 for PSI and 0.9 for PSII. How is this
high efficiency achieved?

ADVANCES:In recent years, structures of
supercomplexes from various algae and plants
have been determined at near-atomic reso-
lution using cryo–electron microscopy. These
structures revealed the pigment-binding ar-
chitecture of many subunits and showed the
static interactions between subunits in detail
for the first time. The biggest surprise was

probably the large variability between organ-
isms in the design of the organization of the
antenna around a highly conserved core.
This is particularly striking for PSI, which can
accommodate many antenna subunits asso-
ciated to the core at positions that can change
between organisms. These differences mainly
reflect adaptation to specific light conditions.
For example, whereas organisms living in water
or in a low-light environment have developed a
large antenna, plants seem to have a smaller

but more modular antenna system to quickly
respond to the typical changes in light intensity
experienced on land.
The processes of EET and CS in some of
these supercomplexes and their subcomplexes
have been studied with a variety of time-
resolved spectroscopic techniques. The excited-
state kinetics of these complexes can now be
related to the structures to reveal the preferred
EET pathways and possible bottlenecks of the
process. This leads to, for example, the sur-
prising conclusion that excitations created in
the major light-harvesting complex of plants
and green algae are not always transferred to
the RCs through the minor antenna complexes,
but rather, several parallel transfer pathways
exist that may facilitate regulatory processes.
It is also becoming clear that the antenna of
PSI can become substantially larger than
that of PSII while maintaining a high quan-
tum efficiency.

OUTLOOK:The high-resolution structures of
the supercomplexes of plants and algae rep-
resent an excellent starting point for study-
ing energy flow in detail
using advanced modeling.
Complexes such as plant PSI
have been studied in detail
by spectroscopy, but little is
known about the functional
behavior of most of the algal
supercomplexes. Spectro-
scopic measurements on these
complexes are now required
to relate structure to func-
tionality. All supercomplexes
in vivo are embedded in the
very crowded environment
of the thylakoid membrane,
where they can interact with
each other, so the next step is
to study the complexes in
their natural environment.
The combination of struc-
tural biology, advanced spec-
troscopy, and modeling will
provide a molecular under-
standing of light harvesting
and its regulation in phys-
iologically relevant condi-
tions. These insights will
also provide a basis for
rational redesign of the photosynthetic appa-
ratus, which could yield increases in crop
productivity.▪

RESEARCH


Croceet al.,Science 369 , 933 (2020) 21 August 2020 1of1


The list of author affiliations is available in the full article online.
*Corresponding author. Email: [email protected]
Cite this article as R. Croce, H. van Amerongen,Science 369 ,
eaay2058 (2020). DOI: 10.1126/science.aay2058

READ THE FULL ARTICLE AT
https://doi.org/10.1126/science.aay2058

10 ns

EET Chl b to Chl a in complex

Equilibration
within complexes

PSI core PSI - LHCI PSIIC 2 S 2

Excited
EET Car to Chl state decay

EET between
complexes
via Chl b

1 ps 10 ps 100 p100 p100 pss 1 ns

CS in the RCs

PSIIC 2 S 2 M 2 PSII C 2 S 2 M 2 N 2

EET between complexes via Chl a

PSII core

100 fs

Timeline of light-harvesting processes.(Top) Many transfer steps between carotenoid and chlorophyll (Chl)aandbmolecules
occurring on different time scales eventually lead to CS and trappingin the RCs. Transfer between complexes occurs mainly through Chl
aand not Chlb. (Bottom) Together, these individual steps determine the average trapping times in the PSI and PSII supercomplexes.

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