Interplay of microbial interaction and biofilm mechanics govern biofilm dynamics

Biofilms are highly structured, densely packed bacterial consortia where many different species can coexist. During biofilm development and growth, the different species often form spatial distribution patterns that govern biofilm composition and function. In some cases, emerging structures have been explained as the result of social interactions between bacteria, e.g. cooperation and competition. Others emphasize the role of local mechanics, where spatial structuring arises from forces exerted between cells or between cells and their environment. Typically, these two lines of argumentation are treated separately. Here, we show that mechanics and social interactions can be strongly interrelated and their combination can crucially impact biofilm formation and dynamics. Using confocal microscopy and bacterial co-culture assays, we examine how bacterial antagonism impacts biofilm mechanics, and vice versa. We study competing Vibrio cholerae strains that kill on contact using the Type 6 secretion system. In case of mutual killers, i.e. two V. cholerae strains that can kill each other on contact, this social interaction leads to the formation of clonal domains of the competing strains (Mc Nally et al., Nat Commun, 2017). Intuitively, an unequal fight may enable a superior killer to invade and quickly eliminate a much weaker competitor. However, we observe that killer cells can coexist with killing-deficient target cells for very long times, and find that this results from the mechanical consequences of the deadly competition. Killing produces dead cells, which accumulates between domains of competing cells and prevents subsequent killing. Counterintuitively, our results suggest that antagonistic interactions stabilize coexistence in diverse communities. The findings demonstrate that the impact of social interactions in bacterial consortia is complex, requiring the understanding of the structural and the statistical-mechanical processes in biofilms.