Predator-prey dynamics of <i>Vibrio cholerae</i> on chitin suggest an alternative mode of biofilm formation in marine snow conditions

Vibrio cholerae is a ubiquitous marine bacterium that solubilizes and consumes chitin in the marine water column. In both the marine environment and the intestinal track, V. cholerae forms biofilms: how do the diverse surfaces that V. cholerae encounters influence its biofilm formation and, in turn, shape its ecological interactions with other microbes? Here, we use the interaction between the predator Bdellovibrio bacteriovorus and V. cholerae as a model to explore how the environmental chitin substrate alters V. cholerae biofilm formation and predator-prey dynamics. We find that glass-bound biofilm growth provides strong protection for V. cholerae against predation while also allowing a population of predatory B. bacteriovorus to remain in place among prey cells. In contrast, chitin-bound biofilm structure offers less protection against B. bacteriovorus predation and does not maintain as stable a population of B. bacteriovorus. Using percolation and population dynamics models, we predict that these changes in predator-prey dynamics can be explained largely by alterations in V. cholerae biofilm architecture between the two conditions, which changes the fraction of prey available to B. bacteriovorus. Using targeted biofilm matrix gene deletions, we confirm this prediction by recapitulating key features of the chitin predator-prey interactions on glass surfaces. Following on this observation, we show that V. cholerae biofilms grown on chitin produce much less of the canonical biofilm matrix components and instead rely on other extracellular structures. Overall, our experiments detail how growth substrate can alter biofilm matrix composition and how these changes in biofilm architecture impact higher-order ecological interactions.