Nutrient availability, along with light and temperature, drives marine primary production. The ability to migrate vertically, a critical trait of motile phytoplankton, allows species to optimize nutrient uptake, storage, and growth. However, this traditional view discounts the possibility that migration in nutrient-limited waters may be actively modulated by the emergence of energy-storing organelles. Here, we report that bloom-forming raphidophytes harness energy-storing cytoplasmic lipid droplets (LDs) to biomechanically regulate vertical migration in nutrient-limited settings. LDs grow and translocate directionally within the cytoplasm, steering strain-specific shifts in the speed, trajectory, and stability of swimming cells. Nutrient reincorporation restores their swimming traits, mediated by an active reconfiguration of LD size and coordinates. A mathematical model of cell mechanics establishes the mechanistic coupling between intracellular changes and emergent migratory behavior. Amenable to the associated photophysiology, LD-governed behavioral shift highlights an exquisite microbial strategy toward niche expansion and resource optimization in nutrient-limited oceans.

The variation associated with different observable characteristics—phenotypes—at the cellular scale underpins homeostasis and the fitness of living systems. However, if and how these noisy phenotypic traits shape properties at the population level remains poorly understood. Here we report that phenotypic noise self-regulates with growth and coordinates collective structural organization, the kinetics of topological defects and the emergence of active transport around confluent colonies. We do this by cataloguing key phenotypic traits in bacteria growing under diverse conditions. Our results reveal a statistically precise critical time for the transition from a monolayer biofilm to a multilayer biofilm, despite the strong noise in the cell geometry and the colony area at the onset of the transition. This reveals a mitigation mechanism between the noise in the cell geometry and the growth rate that dictates the narrow critical time window. By uncovering how rectification of phenotypic noise homogenizes correlated collective properties across colonies, our work points at an emergent strategy that confluent systems employ to tune active transport, buffering inherent heterogeneities associated with natural cellular environment settings.

As open oceans continue to warm, modified currents and enhanced stratification exacerbate nitrogen and phosphorus limitation, constraining primary production. The ability to migrate vertically bestows motile phytoplankton a crucial – albeit energetically expensive – advantage toward vertically redistributing for optimal growth, uptake and resource storage in nutrient-limited water columns. However, this traditional view discounts the possibility that phytoplankton migration may be actively selected by the storage dynamics when nutrients turn limiting. Here we report that storage and migration in phytoplankton are coupled traits, whereby motile species harness energy storing lipid droplets (LDs) to biomechanically regulate migration in nutrient limited settings. LDs grow and translocate directionally within the cytoplasm to accumulate below the cell nucleus, tuning the speed, trajectory and stability of swimming cells. Nutrient reincorporation reverses the LD translocation, restoring the homeostatic migratory traits measured in population-scale millifluidic experiments. Combining intracellular LD tracking and quantitative morphological analysis of red-tide forming alga, Heterosigma akashiwo , along with a model of cell mechanics, we discover that the size and spatial localization of growing LDs govern the ballisticity and orientational stability of migration. The strain-specific shifts in migration which we identify here are amenable to a selective emergence of mixotrophy in nutrient-limited phytoplankton. We rationalize these distinct behavioral acclimatization in an ecological context, relying on concomitant tracking of the photophysiology and reactive oxygen species (ROS) levels, and propose a dissipative mechanical energy budget for motile phytoplankton for alleviating nutrient limitation. The emergent resource acquisition strategies, enabled by distinct strain-specific migratory acclimatizing mechanisms, highlight the active role of the reconfigurable cytoplasmic LDs in vertical movement. By uncovering a mechanistic coupling between dynamics of intracellular changes to physiologically governed migration strategies, this work offers a tractable framework to delineate diverse strategies which phytoplankton may harness to maximize fitness and resource pool in nutrient-limited open oceans of the future.

Phenotypic noise underpins homeostasis and fitness of individual cells. Yet, the extent to which noise shapes cell-to-population properties in microbial active matter remains poorly understood. By quantifying variability in confluent E.coli strains, we catalogue noise across different phenotypic traits. The noise, measured over different temperatures serving as proxy for cellular activity, spanned more than two orders of magnitude. The maximum noise was associated with the cell geometry and the critical colony area at the onset of mono-to-multilayer transition (MTMT), while the lower bound was set by the critical time of the MTMT. Our results, supported by a hydrodynamic model, suggest that a trade-off between the noise in the cell geometry and the growth rate can lead to the self-regulation of the MTMT timing. The MTMT cascades synchronous emergence of hydrodynamic fields, actively enhancing the micro-environmental transport. Our results highlight how interplay of phenotypic noise triggers emergent deterministic properties, and reveal the role of multifield topology-of the colony structure and hydrodynamics-to insulate confluent systems from the inherent noise associated with natural cell-environment settings. Note: The manuscript is supported and accompanied by a Supplementary Information section.

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 akashiwo 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.