Inflation-induced motility for long-distance vertical migration

Abstract

The vertical migrations of pelagic organisms play a crucial role in shaping marine ecosystems and influencing global biogeochemical cycles. They also form the foundation of what might be the largest daily biomass movement on Earth. Surprisingly, among this diverse group of organisms, some single-cell protists can transit depths exceeding 50 m without employing flagella or cilia. How these non-motile cells perform large migrations remains unknown. It has been previously proposed that this capability might rely on the cell's ability to regulate its internal density relative to seawater. Here, using the dinoflagellate algae Pyrocystis noctiluca as a model system, we discover a rapid cell inflation event post cell division, during which a single plankton cell expands its volume 6-fold in less than 10 min. We demonstrate this rapid cellular inflation is the primary mechanism of density control. This self-regulated cellular inflation selectively imports fluid less dense than surrounding seawater and can thus effectively sling-shot a cell and reverse sedimentation within minutes. To accommodate its dramatic cellular expansion, Pyrocystis noctiluca possesses a unique reticulated cytoplasmic architecture that enables a rapid increase in overall cell volume without diluting its cytoplasmic content. We further present a generalized mathematical framework that unifies cell-cycle-driven density regulation, stratified ecology, and associated cell behavior in the open ocean. Our study unveils an ingenious strategy employed by a non-motile plankton to evade the gravitational sedimentation trap, highlighting how precise control of cell size and cell density can enable long-distance migration in the open ocean.