Liquid channels within B. subtilis biofilms allow the escape of trapped clones and population rescue

ABSTRACT

Bacterial communities undergoing spatial expansions, such as colonies and biofilms, typically exhibit a severe loss of genetic diversity due to gene surfing, a phenomenon by which only cells close to the expanding edge have a chance of contributing to the next generation. As a result, mutants that emerge behind the front will remain trapped in the bulk of the population, even if they carry a significant growth advantage. While these findings are applicable to smooth, uniformly dense colonies, where cell spatial re-arrangement is limited, it is unclear whether they hold in bacterial communities that display complex three-dimensional morphologies, such as wrinkly biofilms.

We employ an experimental procedure that enables a rapid switch of the chemical environment with minimal physical manipulation of the cell community to investigate the fate of trapped clones carrying a selective advantage in wrinkly B. subtilis biofilms. We find that these clones are able to use the channels underneath the wrinkles to traverse long distances and take over the expansion front. Moreover, we find that active motility is required to accomplish this task. Collectively, our findings reveal an intriguing novel role of wrinkles, as they enable potentially advantageous mutants to propel themselves towards the leading edge of the expansion and rescue the population upon environmental changes. Our results also point at motility, which has traditionally received little attention in bacterial communities growing on hard substrates, as a key mechanism for population rescue in biofilms that display complex morphologies.