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

Abstract

Microbial communities often respond to environmental cues by adopting collective behaviors--like biofilms or swarming--that benefit the population. Bioconvection is a distinct and robust collective behavior wherein microbes locally gather into dense groups and subsequently plume downward through fluid environments, driving flow and mixing on scales thousands of times larger than an individual cell. Though bioconvection was observed more than 100 years ago, effects of differing physical and chemical inputs, as well as its potential selective advantages to different species of microbes, remain largely unexplored. In the canonical microbial bioconvector Bacillus subtilis, density inversions that drive this flow are setup by vertically oriented oxygen gradients that originate from an air-liquid interface. In this work, we develop Escherichia coli as a complementary model organism for the study of bioconvection. We show that for E. coli and B. subtilis, bioconvection confers a context-dependent growth benefit with clear genetic correlates to motility and chemotaxis. We found that fluid depth, cell concentration, and carbon availability have complimentary effects on the emergence and timing of bioconvective patterns, and whereas oxygen gradients are required for B. subtilis bioconvection, we found that E. coli deficient in aerotaxis ({Delta}aer) or energy-taxis ({Delta}tsr) still bioconvect, as do cultures that lack an air-liquid interface. Thus, in two distantly related microbes, bioconvection confers 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.