per second ( 1 ). In cyanobacteria, the outer
antenna is composed of phycobilisomes: huge,
water-soluble multiprotein complexes anchored
tothemembrane( 17 – 20 )thatarealsopresent
in red algae. In plants and most algae, the
outer antennas are located in the thylakoid
membrane and are members of the light-
harvesting complex (LHC) multigenic family.
Together with the core, they form the PSI and
PSII supercomplexes, which will be addressed
in this review. The plant LHCs all have an
almost identical pigment-protein organization
( 21 ), but they can have very different spectro-
scopic properties (Fig. 2). Each monomer is
composed of an apoprotein of ~25 kDa with
three transmembrane helices and a number
of pigments accounting for another ~15 kDa
(11 to 15 Chls and three to four carotenoid
molecules) (Fig. 2). Although the core com-
plexes, in addition to carotenoids, only bind
Chla, the LHCs of plants and green algae
also bind Chlb, the lowest energy transition
of which is at higher energy than that of Chl
a(Fig. 1). This makes Chlban excellent ex-
citation energy donor for Chla,butanotso
good energy acceptor (Figs. 1 and 3). The Chl
a/bratio varies between antenna complexes
from 1 to 6 but for most of them it is ~2 ( 22 ). The
LHCs of diatoms, called fucoxanthin-binding
proteins (FCPs) (Fig. 2), do not bind Chlb,but
rather Chlc, and they contain fewer Chls (nine
or 10 in total) and more carotenoids (six or seven
fucoxanthins) ( 23 ). Fucoxanthin and Chlcrel-
atively increase the absorption cross section
for blue-green light, which is dominant in a
water environment. Chlcis peculiar because
it lacks the phytol chain that is present in all
other chlorophylls, and this absence allows the
binding of more carotenoids in FCPs (Fig. 2,
inset) ( 24 ).
The structures of the supercomplexes of PSI
( 25 – 27 )andPSII( 28 – 30 ), as well as the num-
ber of associated LHCs, differ substantially. In
plant PSI (Fig. 4), four LHCs (Lhca1 to Lhca4)
are associated with a monomeric core forming
thePSI-LHCIsupercomplex.ThePSIIC 2 S 2 M 2
supercomplex (Fig. 5) instead contains a dimeric
core (C 2 ),andeachcoreisassociatedwiththree
monomeric LHCs (CP29, CP26, and CP24, also
called minor antennas) and two LHCII trimers
called S (strongly bound) and M (moderately
bound). The M-trimer and CP24 are absent in
the smaller version of the plant supercomplex
(C 2 S 2 , Fig. 5), which is the dominant form in
high-light conditions ( 31 ). Slightly different
C 2 S 2 M 2 supercomplexes lacking CP24 have
been observed in conifers ( 32 ), pointing to
variation in structure inside the plant king-
dom. Very recently, cryo–electron microscopy
(cryo-EM) has also provided high-resolution
structures of complexes from various algae.
Although the basic unit is similar in all species
studied, the organization and the dimension
of the outer antenna differ depending on the
environmental niche where the organisms live
( 33 ). For example, PSI and PSII of the model
green algaChlamydomonas reinhardtii(Figs.
4 and 5) are far larger than those of plants,
containing 10 or 11 antennas per core or even
more ( 34 – 38 ). PSII of diatoms (Chaetoceros
gracilis; Fig. 5), on the other hand, has a similar
overall organization as the plant complex but
contains more subunits (up to 35) and the
outer antennas (FCPs) form tetramers instead
of trimers ( 39 , 40 ).
Thesupercomplexstructureshaverecently
been used as a starting point for molecular
dynamics simulations to unveil channels for
the oxidized or reduced quinones entering or
leaving the RCs, respectively ( 41 ), or for protonsthat leave PSII after water splitting has oc-
curred ( 42 ). Conversely, pathways for excita-
tion energy transfer (EET) to the RC are less
specific in the sense that many pigments can
transfer their excitation energy to different
neighbors, thereby creating a multitude of
transfer pathways to the RC. Detailed modeling
of EET in the photosystems might be per-
formed using advanced quantum-mechanical
methods that were applied to early models of
the PSII supercomplexes ( 43 , 44 )butnotyetto
the new structures. Therefore, we will use a
simplified and more intuitive approach to
discuss EET in the supercomplexes.Chlb molecules limit free diffusion of
excitation energy
A crucial parameter for the rate of EET be-
tween two pigments is their mutual distance.
In the LHCs, most nearest neighbors within
one complex are ~10 Å from each other and
show strong electrostatic (excitonic) interac-
tions, which lead to extremely fast EET. EET
in individual complexes has been studied ex-
tensively, showing that within a few hundred
femtoseconds after Chlbexcitation, most of
the excitations are already localized on Chla
molecules ( 33 , 45 – 47 ), which are lower in energy
(Box 1 and Fig. 1). EET within individual
complexes has been modeled with quantum-
mechanical methods, and the light-harvesting
properties of these complexes are now rela-
tively well understood, particularly those of
LHCII ( 16 , 45 , 48 ). On the other hand, EET
from a Chlbmolecule on one complex to a Chl
molecule on a neighboring complex, which are
in general more than 15 Å apart, is far slower,
typically ~10 to 20 ps (Fig. 3). The effective
time of transfer from one complex to the other
through such a Chlb–Chladonor-acceptorCroceet al.,Science 369 , eaay2058 (2020) 21 August 2020 2of9
Chl aS 1SnS 0
Chl akaaSnEnergyS 0SnS 1Light absorptionInternal conversionChl b Carotenoidkba= 1.66κ^2 /R^6 ps^1
kab= 0.19κ^2 /R^6 ps^1
kaa= 5.59κ^2 /R^6 ps^11.909 eV
(650 nm)1.838 eV
(670 nm)400 500 600 700 8000Absorptionwavelength (nm)Chl a
Chl b
Chl d
Chl f
Chl c2
-carotene400 500 600 700 8000Absorptionwavelength (nm)Chl a
Chl b
Chl d
Chl f
Chl c2
-caroteneFig. 1. Properties of photosynthetic pigments. Left, energy diagram. Right, absorption spectra. See Box 1 for details.
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