Bacterial bioconvection confers context-dependent growth benefits and is robust under varying metabolic and genetic conditions

Abstract

ABSTRACT Microbes often respond to environmental cues by adopting collective behaviors—like biofilms or swarming—that benefit the population. During “bioconvection,” microbes gather in dense groups and plume downward through fluid environments, driving flow and mixing on the scale of millions of cells. Though bioconvection was observed a century ago, the effects of differing physical and chemical inputs and its potential selective advantages for different species of microbes remain largely unexplored. In Bacillus subtilis , vertical oxygen gradients that originate from air-liquid interfaces create cell-density inversions that drive bioconvection. Here, we develop Escherichia coli as a complementary model for the study of bioconvection. In the context of a still fluid, we found that motile and chemotactic genotypes of both E. coli and B. subtilis bioconvect and show increased growth compared to immotile or non-chemotactic genotypes, whereas in a well-mixed fluid, there is no growth advantage to motility or chemotaxis. We found that fluid depth, cell concentration, and carbon availability affect the emergence and timing of bioconvective patterns. Also, whereas B. subtilis requires oxygen gradients to bioconvect, E. coli deficient in aerotaxis (Δ aer ) or energy-taxis (Δ tsr ) still bioconvects, as do cultures that lack an air-liquid interface. Thus, in two distantly related microbes, bioconvection may confer context-dependent growth benefits, and E. coli bioconvection is robustly elicited by multiple types of chemotaxis. These results greatly expand the set of physical and metabolic conditions in which this striking collective behavior can be expected and demonstrate its potential to be a generic force for behavioral selection across ecological contexts. IMPORTANCE Individual microorganisms frequently move in response to gradients in their fluid environment, with corresponding metabolic benefits. At a population level, such movements can create density variations in a fluid that couple to gravity and drive large-scale convection and mixing called bioconvection. In this work, we provide evidence that this collective behavior confers a selective benefit on two distantly related species of bacteria. We develop new methods for quantifying this behavior and show that bioconvection in Escherichia coli is surprisingly robust to changes in cell concentration, fluid depth, interface conditions, metabolic sensing, and carbon availability. These results greatly expand the set of conditions known to elicit this collective behavior and indicate its potential to be a selective pressure across ecological contexts.