Background-dependent sensory bet-hedging in chemotactic bacteria

Phenotypic diversity allows populations to hedge their bets when future conditions are uncertain. But how should populations distribute phenotypes when they are certain about some environmental cues but not others? Previous studies measuring cell-to-cell variability in sensitivity to attractants revealed that the chemotaxis network of Escherichia coli, can switch between a high diversity bet-hedging regime, and a low diversity tracking regime for a signal as that signal becomes prevalent. Here, we combine mathematical modeling and single-cell FRET experiments to show that populations of chemotactic bacteria make this transition for each ligand independently. That is, transitioning to tracking one ligand does not compromise the population’s ability to hedge its bets across other future ligands. Remarkably, we found that populations maintain this bet-hedging capability even if the background and foreground ligands compete for receptor binding sites. We explain the independence of the transition between two diversity regimes in chemotaxis with a simple allosteric model of chemoreceptor clusters with precise adaptation. We then extend our model to show that the same effects of background stimuli on diversity arise in simple feed-forward signaling architectures in the perfectly-adapting regime. Our findings shed light on general properties of signaling architecture that allows populations to independently modulate the degree of phenotypic diversity in response to environmental conditions.