A type VII secretion system toxin functioning as a biofilm-specific intercellular signal in Bacillus subtilis

Abstract

Biofilms are cooperative bacterial communities, in which diffusible signal-mediated quorum sensing coordinates the activities of member cells. However, limited diffusion in extracellular polymeric substance (EPS)-filled biofilms suggests existence of another intercellular signaling mechanism that is more adapted to the biofilm environment. Here, I demonstrate that the yfjA operon of Bacillus subtilis encodes one such signaling mechanism. The yfjA operon was induced by the two-component system DegSU, which controls biofilm development. Deleting the yfjA operon resulted in increased expression of DegSU-regulated genes under nutrient-rich conditions, hastening the onset of sporulation in biofilms. The yfjA operon encoded the type VII secretion system effector toxin YFJ in addition to its related proteins. YFJ toxin-mediated intercellular competition required EPS components which promote close cell-cell association, suggesting that the contact-dependent YFJ toxin system functions specifically in biofilms. The YFJ toxin also functioned as an intercellular signal that controlled the activity of DegSU. I propose that the YFJ toxin system is a biofilm-specific intercellular signaling mechanism that controls cell fate in biofilms in response to nutrient conditions and population size.