Inflation induced motility for long-distance vertical migration

Abstract

Living 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. Our work on cellular levitation emphasizes the critical role of studying cell and evolutionary biology in its planetary context.

Direct quantification of unicellular algae sinking velocities reveals cell size, light, and nutrient-dependence

“…can swim faster than the measured sinking velocities 40 , making upward migration from deeper ocean layers possible, given sufficient energy supply, which the accumulated carbohydrates can supply. Such ability of algae to vertically migrate long (~100 m) distances has been suggested before 2,41 , especially for non-motile species 2,15,16,42 . We therefore propose that the regulation of gravitational sinking in motile algae could impact marine carbon and nutrient fluxes, and this should be accounted for when modeling the marine nutrient and carbon fluxes 10,11 .…”

“…In motile species, the ⅔-power law scaling of cell sinking may force larger cells to consume more energy to counteract excessive sinking. Because cell size increases in coordination with cell cycle progression [35][36][37] , the size-dependent sinking within a species can also result in cell cycledependent vertical positioning of the cells in the ocean, as seen in some non-motile species 15 .…”

“…To adjust their vertical position, algae can alter their gravitational sinking and motility, but live cell sinking and sedimentation rate measurements cannot decouple gravitational sinking from motility. Consequently, studies on gravitational sinking have focused on nonmotile species, which can adjust their gravitational sinking by regulating cell size and composition [13][14][15][16][17] . The extent to which gravitational sinking is regulated in motile species remains unclear, and the molecular mechanism(s) responsible for such sinking regulation are unknown even in most non-motile species.…”

Morphodynamics of chloroplast network control light-avoidance response in the non-motile dinoflagellatePyrocystis lunula

“…Structured metamaterials, like this chloroplast morphology, facilitate buckling and other complex deformations [45,46], enabling efficient chloroplast contraction under the confinement of the cell wall. Pyrocystis noctiluca, another species within the Pyrocystis genus, was found to have a reticulated cytoplasm, assisting with the vertical migration [50], showing another intricate link between the morphology of cytoplasmic space and its function in dinoflagellates. We also showed that the dynamics of chloroplast contraction can be effectively modeled using a "visco-elastic" framework with chemically controlled stress applications.…”

“…Pyrocystis spp . are known to live in the lower eutrophic zone at depths of 60 − 100 m [42] and undergo strong diurnal vertical migration [50]. The growth of P. lunula reaches full saturation under low light conditions found at approximately 50 m depth, equivalent to about 12 mW / cm 2 [67].…”