Fine control of chlorophyll-carotenoid interactions defines the functionality of light-harvesting proteins in plants

Abstract

Photosynthetic antenna proteins can be thought of as "programmed solvents", which bind pigments at specific mutual orientations, thus tuning the overall energetic landscape and ensuring highly efficient light-harvesting. While positioning of chlorophyll cofactors is well understood and rationalized by the principle of an "energy funnel", the carotenoids still pose many open questions. Particularly, their short excited state lifetime (<25 ps) renders them potential energy sinks able to compete with the reaction centers and drastically undermine light-harvesting efficiency. Exploration of the orientational phasespace revealed that the placement of central carotenoids minimizes their interaction with the nearest chlorophylls in the plant antenna complexes LHCII, CP26, CP29 and LHCI. At the same time we show that this interaction is highly sensitive to structural perturbations, which has a profound effect on the overall lifetime of the complex. This links the protein dynamics to the light-harvesting regulation in plants by the carotenoids.Photosystem I (PSI) and Photosystem II (PSII) are large, integral membrane protein super-complexes in plants and green algae 1,2 . They are the key components of the light reactions of photosynthesis. While PSII performs water oxidation to build a transmembrane proton gradient and induce electron transfer 3 , PSI primarily produces the universal redox carrier NADPH 4 . From the functional perspective, the photosystem super-complexes are divided into the core sites of actual photochemical reactions, called reaction centers (RCs), and accessory light-harvesting complexes (LHCs). Even though the RC sub-units capture light themselves, the peripheral LHC antenna proteins of the Lhcb (in PSII) and Lhca (in PSI) families are necessary to increase the absorption cross-section and ensure optimal performance 5 . The antenna complexes transfer excitation energy with remarkable efficiency, enabling near unity quantum yield of PSI/II (one photochemical reaction per one photon captured) 6 . This is due to the fine tuning of the relative positions, orientations and excitation energies of chlorophyll (Chl) cofactors coordinated by the residues, which is the reason why LHC proteins are sometimes referred to as "programmed solvent" 2 . The current precision of pigment placement resolved from the crystal structures 7-10 allows for highly detailed models, describing both the initial steps of exciton transfer 11,12 and the subsequent charge separation in the RCs 13 . However, such models largely account only for the Chls, while the second major building block of the pigment arrays, the carotenoids (Cars), are usually disregarded.Cars are typically included in photodynamic models of bacterial systems only, where they are significant light-harvesters 14 , while their light-harvesting role in plants is minor compared to the photoprotective function 15,16 . The latter is performed primarily by quenching the Chl triplet states 17 , which would otherwise sensitize molecular oxygen to form harmful singlet oxy...

Observation of dissipative chlorophyll-to-carotenoid energy transfer in light-harvesting complex II in membrane nanodiscs

“…4a, we resolve the initial rise of Car S 1 ESA, characteristic of a directional energy transfer rather than a delocalized Car-Chl excited state of the excitonic mixing model. Theoretically predicted timescales for this energy transfer pathway are >20 ps due to the optically forbidden nature of the Car S 1 state 43,66,67 , which is two orders of magnitude longer than the sub-ps (<400 fs) timescale observed in our experiment. This discrepancy suggests that a more complex picture is required, such as directional Chl → Car energy transfer mediated by partial mixing of the excited states, along the lines of previous proposals 11,12,19 .…”

Molecular dynamics simulations in photosynthesis

“…Nowadays, different LHC genes from plants, i.e., LHCII Balevičius et al 2017;Thallmair et al 2019), CP29 (Ioannidis et al 2016;Papadatos et al 2017) and PsbS Liguori et al 2019), have been simulated up to the μs timescale with atomistic resolution. Most of these works have focused in particular on characterizing how the interactions among the Chls and Cars bound to LHCs change depending on the different protein conformations sampled via MD (Liguori et al 1 3 2015; Balevičius et al 2017;López-Tarifa et al 2017;Maity et al 2019). This is of particular interest because a change of interactions among Chls or between Chls and Cars can lead to creation or disruption of quenching sites inside the LHCs or can change their spectral properties.…”

“…On the contrary, it was shown that QM methods are necessary to accurately describe changes in Chl-Car couplings along an MD trajectory. Ab initio protocols have been recently developed to compute Chl-Car couplings and also, more specifically, predict the activation of quenching in LHCs (Duffy et al 2013;Balevičius et al 2017;Fox et al 2017;Maity et al 2019). A brief overview of studies using MD simulations in combination with QM methods will be given in Sect.…”

Excitation quenching in chlorophyll–carotenoid antenna systems: ‘coherent’ or ‘incoherent’

“…In order to asses the efficiency of quenching within the dimer and LHCII a suitable measure is needed. Here, as previously (Chmeliov et al 2015;Fox et al 2017Fox et al , 2018Balevičius Jr. et al 2017), we consider the 'mean excitation lifetime', exc . This is an observable quantitiy (through fluorescence lifetime/yield measurements) and is therefore basis-independant.…”