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

Vytautas Balevičius,Christopher D P Duffy,Ingrid G Prandi,Sandro Jurinovich,Benedetta Mennucci,William P Bricker,Kieran F Fox

doi:10.1038/s41598-017-13720-6

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 phase-space 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.

Highlights

Photosystem I (PSI) and Photosystem II (PSII) are large, integral membrane protein super-complexes in plants and green algae[1,2]
The fact that the lifetime of the S1 state is comparable to the typical time-scales of the energy transfer between the protein sub-units[11] raises a conceptual question: How can such pigments be incorporated into a light-harvesting system without hindering its function by wasteful dissipation of the captured energy? Or alternatively, how can such a dissipative channel play a specific integral role in regulating light-harvesting in a fluctuating light environment? In this study we analyze the nearest Chl–Car pairs in the plant antenna complexes LHCII/LHCI, CP26 and CP29 with particular focus on the mutual orientation
We show that within such a configuration, Chl-to-Car excitation transfer rate is highly sensitive to the mutual orientation, which can be driven from excitation-preserving to quenching configurations within physiologically reasonable boundaries

Summary

Introduction

Photosystem I (PSI) and Photosystem II (PSII) are large, integral membrane protein super-complexes in plants and green algae[1,2]. 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 oxygen species[18]. We show that within such a configuration, Chl-to-Car excitation transfer rate is highly sensitive to the mutual orientation, which can be driven from excitation-preserving to quenching configurations within physiologically reasonable boundaries This supports the idea of Cars acting as one of the agents regulating energy density in the photosystems under high-light conditions, and presents the most feasible molecular switching pathway

Methods

Results

Conclusion