Photosynthetic cell under stress: focus on ultrastructure of microalgae

In photosynthetic organisms including unicellular algae, acclimation to and damage by environmental stresses are readily apparent at the level of cell ultrastructural organization and, particularly, organization of the photosynthetic apparatus and cell inclusions. Although the physiological and molecular mechanisms of these processes are well known, the ultrastructural picture of the stress responses is often elusive and frequently controversial. Here, we present the results of quantitative analysis of an extensive set of electron microscopy images of the microalgal cells composed across species of Chlorophyta and in a wide range of growth conditions aligned with well-defined physiological parameters and optical properties. Distinct ultrastructural changes typical of normal functioning, acclimation of the cell and emergency reduction of its chloroplast membrane system under high light exposure and/or mineral nutrient starvation were pinpointed. We also showed the patterns of the stress-related ultrastructural changes including peculiar thylakoid rearrangements and autophagy-like processes. We followed the changes in the chloroplast and the combined area of stroma with thylakoids, oil bodies and starch grains. Special attention was paid to the photosynthetic membrane condition and the topological reorgnization of the chloroplast envelope. The comparative study across a wide range of model stresses and several microalgal species showed common patterns manifesting the reduction of the photosynthetic apparatus under stress and its recovery from the stress. We also attempted to integrate the detailed record of diverse ultrastructural changes into a more general picture of stress acclimation which turned out to be different depending on the level of stress tolerance. Thus, the organisms featuring a high stress tolerance displayed a controlled reduction or even expansion of the photosynthetic apparatus, a safe dissipation of already absorbed light energy, maintenance of photosynthesis and saving resources of carbon, energy, and mineral nutrients ensuring rapid recovery after stress. By contrast, the ultrastructural manifestations of a low stress tolerance reflected an obvious mismatch of light capture by and light energy utilization capacity of the cell calling for the emergency reduction of light interception by the photosynthetic apparatus and occasionally resulting in signs of damage. Collectively, the analysis of ultrastructural data improves our understanding of the generic stress responses of photosynthetic microorganisms. It is also a welcome complement to recent insights into the mechanisms of cell functioning under favorable or stressful conditions obtained by the advanced molecular biology approaches. Financial support of Russian Science Foundation (grant 14-50-00029) is gratefully acknowledged.