• accelerated molecular dynamics
• dimensionality reduction
• electronic energy transfer (EET)
• excitonic model
• light harvesting
• light harvesting complex stress-related (LHCSR)
• molecular dynamics (MD)
• nonphotochemical quenching (NPQ)
• Physcomitrella Patens
• time-lagged Independent Component Analysis (tICA)

Photosystems of plants, mosses and algae, contain Light Harvesting Complexes (LHCs), which are dedicated to absorbing light and transferring the corresponding electronic energy towards reaction centers. LHCs are Pigment-Protein Complexes (PPCs) containing chlorophylls and carotenoids, and are part of both photosystem I (PSI) and II (PSII), which in turn are located the thylakoid membrane of chloroplasts. LHCs are also responsible for dissipating excess energy that is formed under high illumination conditions. They do so through the so-called nonphotochemical quenching (NPQ) process, that is, the non-radiative quenching of chlorophyll excitation. NPQ is a key feature of photoprotection since it prevents harmful oxidative stress, which would compromise the proper execution of the electron transport chain. Growing evidence in literature assesses that the NPQ fastest component, the energy dependent quenching (qE), is triggered from a pH drop in the lumen of the thylakoid caused by high light conditions, switching LHCs to a quenched state. In mosses and algae, a subclass of the LHC family, i.e. the Light Harvesting Complexes Stress Related (LHCSR), is responsible for direct pH sensing and light-harvesting regulation functions. A credited hypothesis is that ionizable amino acid residues exposed to the lumen detect pH variations and then induce a conformational change in the protein scaffold, influencing the arrangement of pigments and their quenching properties. It is generally accepted that carotenoids play a major role in quenching chlorophyll excitation, through the electronic energy transfer (EET) process. However, how this quenching can be turned on or off by conformational changes is still not understood.

In the present work, we aim to gain further understanding of NPQ in the LHCSR1 of the moss Physcomitrella Patens, starting from a computational model of the complex, in terms of EET modulated by the pigments interactions. We analyze enhanced sampling molecular dynamics (MD) trajectories of LHCSR1 corresponding to different protonation states to identify conformational changes that correlate with reduced pH in the lumenal side. Through dimensionality reduction techniques and clustering algorithms, we classify the conformations of LHCSR1 between acidic and neutral conditions. To connect the conformations with the properties of the pigments, we performed Quantum Mechanics/Molecular Mechanics (QM/MM) calculations to study different pigment properties related to their lower excited state. Considering the excitonic approximation, we then estimated the excited-state lifetime of pigments in the different conformations. For this purpose, we used a kinetic model describing the EET process among all pigments of LHCSR1.

The results assess a larger conformational freedom of most protonated LHCSR1 states: each of them corresponds at least to a respective conformation. On the contrary, changes in arrangements and properties of pigments are subtle and do not seem clearly induced by different scaffold structures. In the end, the kinetic model implemented solely reproduces lifetimes typical of a quenched complex, with little variation between the clusters. We consider that EET is still not accurately described, or that another quenching mechanism, namely charge-transfer, can't be neglected in describing qE.