A different perspective for nonphotochemical quenching in plant antenna complexes

Edoardo Cignoni,Benedetta Mennucci,Silvia Acosta-Gutiérrez,Francesco Luigi Gervasio,Margherita Lapillo,Lorenzo Cupellini

doi:10.1038/s41467-021-27526-8

Abstract

Light-harvesting complexes of plants exert a dual function of light-harvesting (LH) and photoprotection through processes collectively called nonphotochemical quenching (NPQ). While LH processes are relatively well characterized, those involved in NPQ are less understood. Here, we characterize the quenching mechanisms of CP29, a minor LHC of plants, through the integration of two complementary enhanced-sampling techniques, dimensionality reduction schemes, electronic calculations and the analysis of cryo-EM data in the light of the predicted conformational ensemble. Our study reveals that the switch between LH and quenching state is more complex than previously thought. Several conformations of the lumenal side of the protein occur and differently affect the pigments’ relative geometries and interactions. Moreover, we show that a quenching mechanism localized on a single chlorophyll-carotenoid pair is not sufficient but many chlorophylls are simultaneously involved. In such a diffuse mechanism, short-range interactions between each carotenoid and different chlorophylls combined with a protein-mediated tuning of the carotenoid excitation energies have to be considered in addition to the commonly suggested Coulomb interactions.

Highlights

Light-harvesting complexes of plants exert a dual function of light-harvesting (LH) and photoprotection through processes collectively called nonphotochemical quenching (NPQ)
By combining two complementary enhanced sampling techniques[30,31] with unbiased molecular dynamics simulations[32,33] and dimensionality reduction methods, we thoroughly explore the conformational landscape of the complex and establish how the apoprotein conformation impacts the L1 and L2 sites and the interactions among the embedded pigments
The conformational sampling of CP29 is here enhanced by employing parallel tempering in the well-tempered ensemble (PT-WTE)[34,35]

Summary

Introduction

Light-harvesting complexes of plants exert a dual function of light-harvesting (LH) and photoprotection through processes collectively called nonphotochemical quenching (NPQ). We show that a quenching mechanism localized on a single chlorophyll-carotenoid pair is not sufficient but many chlorophylls are simultaneously involved In such a diffuse mechanism, short-range interactions between each carotenoid and different chlorophylls combined with a protein-mediated tuning of the carotenoid excitation energies have to be considered in addition to the commonly suggested Coulomb interactions. The main strategy is to dissipate the energy absorbed by chlorophylls into harmless heat; this is made possible through processes collectively called nonphotochemical quenching (NPQ)[3–8]. Most authors agree that the carotenoid molecules (Cars) embedded in LHCs actively participate in the quenching[9–11] Within this hypothesis, the most widely accepted mechanism for the quenching involves excitation energy transfer (EET) from the excited Chls to the dark (S1) state of Cars[9,12].

Methods

Results

Conclusion