Intercellular positive-feedback loops promote the evolutionary stability of microbial cooperative behaviors

Abstract

AbstractMicrobial cooperation enables groups of conspecific cells to perform tasks that cannot be performed efficiently by individual cells, such as utilization of various secreted ‘public-good’ molecules, communication via quorum-sensing, or the formation of multicellular structures. Cooperation is often costly and therefore susceptible to exploitation by ‘cheater’ cells, which enjoy the benefit of cooperation without investing in it. While population structure is key to the maintenance of cooperation, it remains unclear whether other mechanisms help in stabilizing microbial cooperation. Like other microbial traits, cooperation is often governed by complex regulatory networks, and one reoccurring motif is an ‘intercellular positive-feedback loop’, where a secreted molecule, e.g. a public-good or a quorum-sensing signaling molecule, activates its own production in all surrounding cells. Here we investigate the role of intercellular feedbacks in the maintenance of bacterial cooperation. We combine theory with a synthetic-biology approach, using swarming motility ofBacillus subtilisengineered variants, to compare the response of ‘open-loop’ and feedback cooperators to the presence of cheaters. We find that positive feedbacks on cooperative behaviors – either directly or through a feedback on quorum-sensing – maintain cooperation in a broader range of environments, relieving the requirement for a strong population structure. Our results directly demonstrate the stabilizing effect of intercellular positive feedbacks on cooperative behaviors, and suggests an explanation for their abundance in regulatory networks of bacterial cooperation.