Asymmetric survival in single-cell lineages of cyanobacteria in response to photodamage

Abstract

Oxygenic photosynthesis is driven by the coupled action of the light-dependent pigment protein complexes, photosystem I and II, located within the internal thylakoid membrane system. However, photosystem II is known to be prone to photooxidative damage. Thus, photosynthetic organisms have evolved a repair cycle to continuously replace the damaged proteins in photosystem II. However, it has remained difficult to deconvolute the damage and repair processes using traditional ensemble approaches. Here we demonstrate an automated approach using time-lapse fluorescence microscopy and computational image analysis to study the dynamics and effects of photodamage in single cells at sub-cellular resolution in cyanobacteria. By growing cells in a two-dimensional layer, we avoid shading effects, thereby generating uniform and reproducible growth conditions. Using this platform, we analyzed the growth and physiology of multiple strains simultaneously under defined photoinhibitory conditions stimulated by UV-A light. Our results reveal an asymmetric cellular response to photodamage between sibling cells and the generation of an elusive subcellular structure, here named a photoendosome, derived from the thylakoid which could indicate the presence of a previously unknown photoprotective mechanism. We anticipate these results to be a starting point for further studies to better understand photodamage and repair at the single-cell level.