Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence

Turbulence is an important determinant of phytoplankton physiology, often leading to cell stress and damage. Turbulence affects phytoplankton migration both by transporting cells and by triggering switches in migratory behavior, whereby vertically migrating cells can actively invert their direction of migration upon exposure to turbulent cues. However, a mechanistic link between single-cell physiology and vertical migration of phytoplankton in turbulence is currently missing. Here, by combining physiological and behavioral experiments with a mathematical model of stress accumulation and dissipation, we show that the mechanism responsible for the switch in the direction of migration in the marine raphidophyte Heterosigma akashiwo is the integration of reactive oxygen species (ROS) signaling generated by turbulent cues. Within timescales as short as tens of seconds, the emergent downward-migrating subpopulation exhibited a twofold increase in ROS, an indicator of stress, 15% lower photosynthetic efficiency, and 35% lower growth rate over multiple generations compared to the upward-migrating subpopulation. The origin of the behavioral split as a result of a bistable oxidative stress response is corroborated by the observation that exposure of cells to exogenous stressors (H2O2, UV-A radiation, or high irradiance), in lieu of turbulence, caused comparable ROS accumulation and an equivalent split into the two subpopulations. By providing a mechanistic link between the single-cell mechanics of swimming and physiology on the one side and the emergent population-scale migratory response and impact on fitness on the other, the ROS-mediated early warning response we discovered contributes to our understanding of phytoplankton community composition in future ocean conditions.

Metabolic homeostasis controls the diversity of cooperative swarming in pathogenic bacteria

Many bacteria have an incredible ability to swarm cooperatively over surfaces. But swarming phenotypes can be quite different even between strains of the same species. What drives this diversity? We compared the metabolomes of 29 clinical Pseudomonas aeruginosa isolates with a range of swarming phenotypes. We identified that isolates incapable of secreting rhamnolipids—a surfactant needed for swarming—had perturbed tricarboxylic acid (TCA) cycle and amino acid pathways and grew exponentially slower in glycerol minimal medium. Analysis of the metabolome signatures and simulations using a genome-scale model led to a mechanism which joins these observations: Strains subject to higher oxidative stress levels grow slower and shut down rhamnolipids secretion, a carbon overflow mechanism possibly to direct carbon resources towards costly stress response pathways to maintain cell viability. In vitro experiments confirmed that rhamnolipid non-producers deal worse with oxidative stress, linking intracellular redox homeostasis—a individual-level trait—to swarming—a population-level behavior. This mechanism helps explain the metabolic constraints on bacteria when secreting byproducts to interact with others—competitively and cooperatively—in microbial communities.SignificanceSwarming motility has been associated with virulence of many human bacterial pathogens. The pathogen Pseudomonas aeruginosa swarms by cooperatively secreting surfactants called rhamnolipids to lubricate surfaces. To understand why some P. aeruginosa strains swarm and others do not, we combined metabolomics, computational modeling and in vitro experiments to study the different swarming behaviors of 29 isolates of Pseudomonas aeruginosa obtained from infected patients. We found that strains can only produce rhamnolipids if they can maintain redox homeostasis. We propose that single cells must have low internal redox stress levels before they can produce rhamnolipids, which work as an overflow of carbon metabolism into a cooperative secretion that brings a fitness benefit to the entire swarming population. This mechanism links single-cell physiology and a population-level cooperative behavior key to the fitness and virulence of P. aeruginosa, a major source of hospital acquired infections.SynopsisThis study combined metabolomics, computational modeling and experiments to explain the swarming diversity in Pseudomonas aeruginosa, yielding new insights on the genetic and metabolic controls of bacterial swarming behaviorRhamnolipid secretion is necessary, but insufficient, for swarmingP. aeruginosa strains unable to produce rhamnolipids in the glycerol minimal medium have perturbed metabolism, slow growth and elevated oxidative stressRhamnolipid producers cannot produce rhamnolipids in succinate as the sole carbon source which causes greater ROS (reactive oxygen species) productionThe requirement of redox homeostasis for rhamnolipid production ensures that the overflow of precious carbon for population-level benefit is prudently controlledThis study helps linking single cell physiology with collective behavior key to the fitness and virulence of a pathogenic bacterium.

Bistability in oxidative stress response determines the migration behavior of phytoplankton in turbulence

Turbulence is an important determinant of phytoplankton physiology, often leading to cell stress and damage. Turbulence affects phytoplankton migration, both by transporting cells and by triggering switches in migratory behavior, whereby vertically migrating cells can invert their direction of migration upon exposure to turbulent cues. However, a mechanistic link between single-cell physiology and vertical migration of phytoplankton in turbulence is currently missing. Here, by combining physiological and behavioral experiments with a mathematical model of stress accumulation and dissipation, we show that the mechanism responsible for the switch in the direction of migration in the marine raphidophyte Heterosigma akashiwo is the integration of reactive oxygen species (ROS) signaling generated by turbulent cues. Within timescales as short as tens of seconds, the emergent downward-migrating subpopulation exhibited a two-fold increase of ROS, an indicator of stress, 15% lower photosynthetic efficiency, and 35% lower growth rate over multiple generations compared to the upward-migrating subpopulation. The origin of the behavioral split in a bistable oxidative stress response is corroborated by the observation that exposure of cells to exogenous stressors (H2O2, UV-A radiation or high irradiance), in lieu of turbulence, caused comparable ROS accumulation and an equivalent split into the two subpopulations. By providing a mechanistic link between single-cell physiology, population-scale migration and fitness, these results contribute to our understanding of phytoplankton community composition in future ocean conditions.Significance StatementTurbulence has long been known to drive phytoplankton fitness and species succession: motile species dominate in calmer environments and non-motile species in turbulent conditions. Yet, a mechanistic understanding of the effect of turbulence on phytoplankton migratory behavior and physiology is lacking. By combining a method to generate turbulent cues, quantification of stress accumulation and physiology, and a mathematical model of stress dynamics, we show that motile phytoplankton use their mechanical stability to sense the intensity of turbulent cues and integrate these cues in time via stress signaling to trigger switches in migratory behavior. The stress-mediated warning strategy we discovered provides a paradigm for how phytoplankton cope with turbulence, thereby potentially governing which species will be successful in a changing ocean.

Technical bias of microcultivation environments on single-cell physiology

The cross-platform comparison of three different single-cell cultivation methods demonstrates technical influences on biological key parameters like specific growth rate, division rate and cellular morphology.

Neural Systems for Spatial Attention in the Human Brain

Spatial attention has been studied for over a half a century. Early behavioural work showed that attending to a location improves performance on a variety of tasks. Since then substantial progress has been made on understanding the neural mechanisms underlying these effects. This chapter reviews the neuroimaging literature, as well as related behavioural and single-cell physiology studies, on visual spatial attention. In particular, the chapter frames much of the work in the context of the biased competition theory of attention, which argues that a primary mechanism of attention is to bias competition among stimuli in the visual cortex in favour of an attended stimulus that, as a result, receives enhanced processing to guide behaviour. Accordingly, the authors have organized this chapter into two related sections. The first summarizes the effects of attention in the visual cortex and thalamus, the so-called ‘site’ of attention. The second explores the relationship between attention and fronto-parietal mechanisms which are thought to be the ‘source’ of the biasing signals exerted on the visual cortex.