Biophysical and molecular mechanisms responsible for phytoplankton sinking in response to starvation

Marine phytoplankton face eco-evolutionary pressure to regulate their vertical position in the ocean to access light, which is abundant towards the surface, and nutrients, which are found deeper down the water column. All phytoplankton experience gravitational sinking, which can contribute to their vertical migration. However, the biophysical and molecular mechanisms that impact gravitational sinking have not been systematically characterized across taxa and environmental conditions. Here, we combine simulations and experiments to investigate the effects of nutrient availability on gravitational sinking in 9 diverse species of unicellular eukaryotic marine phytoplankton. Using measurements of cell mass, volume, and molecular composition, we find that most phytoplankton increase their gravitational sinking when starved, but the biophysical basis for the altered sinking varies across species and starvation conditions. For example, Chaetoceros calcitrans relies nearly exclusively on density regulation whereas Emiliania huxleyi relies on volume regulation. On the molecular level, the observed sinking changes are predominantly attributed to cellular dry contents, rather than water content. For example, starch accumulation increases sinking in 3 green algae species, and lipid accumulation decreases sinking in Phaeodactylum tricornutum . Overall, our work suggests that the evolution of phytoplankton physiology has found multiple biophysical and molecular solutions to support the vertical migration of the cell.