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.