A topologically complex cytoplasm enables inflation-based escape from a gravity trap

Abstract

AbstractLiving cells evolve under specific ecological conditions. The mass of our planet setting a constant gravitational pull and its daily rotation on its axis setting a circadian rhythm are two examples of universal ecological parameters that shape the physiology of every living creature on earth. In the ocean, gravity plays a critical role in shaping the life history of phytoplankton with vast diversity of size and cell geometries all depending on light to survive while gravity is pulling them down. In order to survive, these organisms must evolve means to navigate a vertically stratified ocean. Here we present how cellular topology can enable sinking, rising, and levitation dynamics of seemingly non-motile cells in the open ocean. By studying the bio-luminescent dinoflagellate Pyrocystis noctiluca, we discover how rapid inflation dynamics regulates cell size and buoyancy in coordination to its cell cycle. Live-cell light-sheet imaging reveals a (n-genus) toroidal cytoplasm that enables this rapid inflation of overall cell volume over 5 fold in 15 minutes without dilution of cytoplasmic contents. Here we present combined field and lab measurements with system modeling to build a general framework for how non-motile plankton can escape the gravitational sedimentation trap, and how precise control of cell size becomes essential to survival. Our work on cellular levitation emphasizes the critical role of studying cell and evolutionary biology in its planetary context.