Light-regulated chloroplast morphodynamics in a single-celled dinoflagellate

Photosynthetic algae play a significant role in oceanic carbon capture. However, their performance is constantly challenged by fluctuations in environmental light conditions. While phototaxis is a common strategy to cope with such fluctuations, nonmotile species must adopt alternative mechanisms to avoid light-induced damage. Here, we show that the nonmotile, single-celled marine dinoflagellate Pyrocystis lunula contains a chloroplast network that undergoes strong deformation in response to strong light. By exposing cells to various physiologically relevant light conditions and applying temporal illumination sequences, we find that the light-induced network morphodynamics follows dynamic rules similar to temporal low-pass filtering. We develop a mathematical formalism to model the light-regulated behavior, exposing the relevant timescales of the morphodynamic response. Moreover, confocal microscopy reveals that the unusual reticulated morphology exhibits properties similar to auxetic metamaterials, facilitating the rapid and drastic deformation necessary for the light-avoidance motion, confined by the cell wall. This mechanism reduces the effective chloroplast area under high light conditions, minimizing light absorption and preventing photodamage. Our findings demonstrate that the intricate connection between the chloroplasts topologically complex structure and active dynamics enables the dinoflagellate's dynamic adaptation to changing light environments, thereby supporting essential life-sustaining processes.