A topologically complex cytoplasm enables inflation-based escape from a gravity trap
The daily vertical migrations of plankton play a crucial role in shaping marine ecosystems and influencing global biogeochemical cycles. They also form the foundation of the largest daily biomass movement on Earth. Surprisingly, amongst this diverse group of organisms, some single cell protists transit these depths exceeding 50 meters without employing flagella or cilia, and the underlying mechanisms remain poorly understood. It has been previously proposed that this capability relies on the cells ability to regulate its internal density relative to seawater. Here, using Pyrocystis noctiluca as a model system, we demonstrate the primary mechanism for this density control is a rapid cellular inflation event, during which a single plankton cell expands its volume six-fold in less than 10 minutes. This self-regulated cellular inflation selectively imports fluid less dense than surrounding seawater, and can effectively sling-shot a cell and reverse sedimentation within minutes. This ability is made possible by a reticulated cytoplasmic architecture in Pyrocystis noctiluca that enables this rapid increase in overall cell volume without dilution of 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 non-motile plankton to evade the gravitational sedimentation trap, highlighting how precise control of cell size was essential for survival in the ocean.