Computational modelling of the molecular processes at the heart of adaptable natural light-harvesting.

Significance and timeliness: Photosynthetic organisms possess the capacity for highly efficient light-harvesting. Such efficiency, unequalled by artificial solar devices, is facilitated by the antenna/reaction centre architecture of the photosynthetic membrane. The antenna - a large modular assembly of various pigment-binding proteins - serves to capture spectrally-varied and often spatially-diffuse solar energy and deliver it the photosynthetic reaction centres (RCs). However, efficiency is not the only design principle governing light-harvesting architecture. Photosynthetic organisms are often faced with rapid and large fluctuations in light intensity. In high light an efficient antenna can be a liability as it can lead to a build-up of a potentially harmful excess of excitation energy in the photosynthetic membrane, resulting in a long-term reduction in photosynthetic productivity (photoinhibition). Rapid, photoprotective adaptability to changing light conditions is therefore a vital feature of the photosynthetic membrane.
The challenges associated with a rapidly changing climate and a pressing need for the development of viable solar technology mean that a detailed knowledge of the molecular mechanisms that enable efficient and adaptable natural light-harvesting is of paramount importance for the development of smart, bio-mimetic solar technology, for the prediction of the ecological and agricultural impact of climate change, and for the artificial improvement of photosynthetic productivity during periods of drastic environmental perturbations.

Subject: The component of the photosynthetic membrane most vulnerable to intense light is Photosystem II. The light-harvesting architecture of PSII in plants possesses an almost unique level of adaptive flexibility [1]. Through this flexibility the photosystem can defend itself against intense light via the creation of dissipative pathways within the antenna that trap excess excitation energy and harmlessly dissipate it as heat, a process known as non-photochemical quenching (NPQ). The primary driving force behind this mechanism is the formation of a trans-membrane proton gradient which alters the structural state of the individual antenna complexes (the intrinsic switch) and the spatial organisation of the modular components of PSII (the dynamic membrane) [2]. This multi-scale dynamic alteration leads to the formation of the dissipative energy transfer pathways that relieve the RCs from over-excitation and damage.

Problem and objectives: Computational modelling of the energy transfer dynamics of individual light-harvesting complexes (LHCs) has revealed much about the inter-molecular interactions responsible for excitation dissipation [3]. However, nothing is known about the dynamics and photo-physical/biological significance of the intrinsic switch and the dynamic membrane. The aim of the project is therefore to reveal the molecular mechanisms that drive these structural changes and provide a detailed molecular picture of solar energy capture, transfer and dissipation in the dynamic photosynthetic membrane.

Project outline: The project involves constructing a multi-scale computational model of the PSII membrane. The dynamics of the intrinsic switch in individual LHCs will be modelled via detailed molecular dynamics (MD) simulations. Molecular factors proposed to determine the internal conformational state are the interactions between surface-exposed regions of the membrane proteins and protons and the preferential binding of the pigment violaxanthin/zeaxanthin in dark/light (the xanthophyll cycle). This model will reveal how environmental factors determine the intrinsic conformational state of the LHCs and the kinetics of transition between states. This model will then be coupled to a quantum chemical model of the energy transfer dynamics of these complexes, yielding the first molecular picture of the regulation of light-harvesting at the molecular level.
Modelling of the intrinsic switch will be incorporated into a model of large-scale protein diffusion within the dynamic membrane via a classical 2D model of protein diffusion in the membrane. Finally, stochastic modelling of long-range energy transfer processes in the dynamic membrane will yield the first complete molecular picture of the dynamic photosynthetic membrane. The philosophy behind this project is outlined in the recent perspective article by the project supervisor [1].

Training and experience: The theoretical project should appeal to students with a degree in a physical sciences subject with interest/experience in theoretical and computational modelling of molecular processes. The student will gain extensive training in the methods of quantum/theoretical chemistry, electronic structure theory, molecular dynamics, stochastic and statistical mechanics, simulation/software development and academic writing and presentation. The supervisor has extensive links to international labs working in theoretical and experimental photosynthesis research and the student will be encouraged to connect with the international research community.