Phytoplankton tune local pH to actively modulate circadian swimming behavior

Diel vertical migration (DVM), the diurnal exodus of motile phytoplankton between the light- and nutrient-rich aquatic regions, is governed by endogenous biological clocks. Many species exhibit irregular DVM patterns wherein out-of-phase gravitactic swimming–relative to that expected due to the endogenous rhythm–is observed. How cells achieve and control this irregular swimming behavior remains poorly understood. Combining local environmental monitoring with behavioral and physiological analyses of motile bloom-forming Heterosigma akaswhiwo cells, we report that phytoplankton species modulate their DVM pattern by progressively tuning local pH, yielding physiologically equivalent yet behaviorally distinct gravitactic sub-populations which remain separated vertically within a visibly homogeneous cell distribution. Individual and population-scale tracking of the isolated top and bottom sub-populations revealed similar gravitactic (swimming speed and stability) and physiological traits (growth rate and maximum photosynthetic yield), suggesting that the sub-populations emerge due to mutual co-existence. Exposing the top (bottom) sub-population to the spent media of the bottom (top) counterpart recreates the emergent vertical distribution, while no such phenomenon was observed when the sub-populations were exposed to their own spent media. A model of swimming mechanics based on the quantitative analysis of cell morphologies confirms that the emergent sub-populations represent distinct swimming stabilities, resulting from morphological transformations after the cells are exposed to the spent media. Together with the corresponding night-time dataset, we present an integrated picture of the circadian swimming, wherein active chemo-regulation of the local environment underpins motility variations for potential ecological advantages via intraspecific division of labor over the day-night cycle. This chemo-regulated migratory trait offers mechanistic insights into the irregular diel migration, relevant particularly for modelling phytoplankton transport, fitness and adaptation as globally, ocean waters see a persistent drop in the mean pH.