Community behaviors of bacteria in flow: Divergent roles for transport and collective morphology

Abstract

AbstractFluid flows are dominant features of many bacterial environments, and flow can often impact bacterial behaviors in unexpected ways1–3. For example, the most common types of cardiovascular infections are heart valve colonization by Gram-positive bacteria likeStaphylococcus aureusandEnterococcus faecalis(endocarditis)4,5. This behavior is seemingly paradoxical because heart valves experience high shear rates that would naively be expected to reduce colonization. To ascertain the mechanisms underlying the ability of these bacteria to preferentially colonize higher shear rate environments, we developed a microfluidic system to quantify the effect of flow conditions on the colonization ofS. aureusandE. faecalis.We find that the preferential colonization in high flow of both species is not specific to heart valves and can be found in simple configurations lacking any host factors. Surprisingly, experimental and computational studies reveal that the two species achieve this behavior via distinct mechanisms.S. aureusgrows in cell clusters and produces a dispersal signal whose transport is affected by shear rate. Meanwhile,E. faecalisgrows in linear chains whose mechanical properties result in less dispersal in the presence of higher shear force. In addition to establishing two divergent mechanisms by which these bacteria each preferentially colonize high-flow environments, our findings highlight the importance of understanding bacterial behaviors at the level of collective interactions among cells. These results suggest that distinct microcolony morphologies have previously unappreciated costs and benefits in different environments, like those introduced by fluid flow.