Thylakoid Ultrastructure: Visualizing the Photosynthetic Machinery

Abstract

The surface of our planet receives ∼3020 ZJ per year of solar energy annually, which is >5000 times the energy required to power our entire global economy (∼0.6 ZJ per year). Of this energy, ∼43% is photosynthetic active light radiation (PAR) that can be used to drive microalgal biotechnologies for the production of food, fuels, high value products, carbon sequestration, and bioremediation. The first step of all light-driven microalgal processes is light capture. A diverse array of highly efficient, self-assembling, light-responsive “solar interfaces,” the thylakoid membranes, have evolved to tap into this abundant, but constantly changing, energy resource to power the biosphere. The photosynthetic machinery within the thylakoids is intricately arranged in a complex 3D architecture and designed to adapt dynamically (i.e., 4D: representing changes in 3D structures over time) to constantly changing environmental conditions, to maximize solar to chemical energy conversion. The ATP and NADPH generated are used to produce the complex set of biomolecules that collectively form biomass. Here, we review the structural organization of these amazing photosynthetic interfaces in the model organism Chlamydomonas reinhardtii and summarize recent advances in structural biology, which underpin the development of next-generation atomic resolution dynamic simulations of these systems. Revealing such a 4D atlas of 3D structures in atomic resolution detail is of fundamental importance to enable structure-guided design of natural photosynthetic systems for biotechnological application and to provide a blueprint for the design of nanoscale components, which are the building blocks for the development of next-generation artificial solar fuel systems.