Growth-dependent sensory bet-hedging enhances collective navigation

Abstract

Phenotypic heterogeneity in microbes can be a double-edged sword -- boosting individual survival in uncertain environments, but potentially compromising beneficial population coordination. Dissecting how microbes resolve this tradeoff is challenging because interactions span multiple scales--from molecular interactions to single-cell behavior, population dynamics, and environmental feedback. Here, we address this question for the Escherichia coli chemotaxis system, which implements both individual motile explorations and collective resource exploitations using the same cellular machinery. We quantify the heterogeneity of individual sensory and behavioral phenotypes, as well as the abundance of key signaling proteins during growth in various environments, and test their impact on population-scale collective migration. We identify growth rate as a key environment-dependent physiological variable governing not only the mean but also the variance of sensory phenotypes. Remarkably, rather than hindering population coordination, we find that sensory diversity benefits collective chemotactic navigation in uncertain environments. Strong heterogeneity of expressed phenotypes enhances readiness to multiple sensory cues, and the required population coordination is achieved by phenotypic filtering of that diversity by the collective behavior itself. These results reveal a sensory bet-hedging strategy for collective navigation during population growth: diversity in sensitivity to nutrients currently being consumed is reduced to promote focused exploitation, while it is increased for nutrients not yet encountered to enhance exploration for new growth opportunities.