A Trimeric Autotransporter Enhances Biofilm Cohesiveness in Yersinia pseudotuberculosis but Not in Yersinia pestis.

Cohesion of biofilms made by and has been attributed solely to an extracellular polysaccharide matrix encoded by the genes (Hms-dependent extracellular matrix [Hms-ECM]). However, mutations in the BarA/UvrY/CsrB regulatory cascade enhance biofilm stability without dramatically increasing Hms-ECM production. We found that treatment with proteinase K enzyme effectively destabilized mutant biofilms, suggesting that cell-cell interactions might be mediated by protein adhesins or extracellular matrix proteins. We identified an uncharacterized trimeric autotransporter lipoprotein (YPTB2394), repressed by , which has been referred to as YadE. Biofilms made by a Δ mutant strain were extremely sensitive to mechanical disruption. Overexpression of in wild-type increased biofilm cohesion, similar to biofilms made by or mutants. We found that the Rcs signaling cascade, which represses Hms-ECM production, activated expression of The gene appears to be functional in but is a pseudogene in modern strains. Expression of functional in KIM6+ weakened biofilms made by these bacteria. This suggests that although the YadE autotransporter protein increases biofilm stability, it may be incompatible with the Hms-ECM production that is essential for biofilm production in fleas. Inactivation of in may be another instance of selective gene loss in the evolution of flea-borne transmission by this species. The evolution of from its ancestor involved gene acquisition and gene losses, leading to differences in biofilm production. Characterizing the unique biofilm features of both species may provide better understanding of how each adapts to its specific niches. This study identifies a trimeric autotransporter, YadE, that promotes biofilm stability of but which has been inactivated in , perhaps because it is not compatible with the Hms polysaccharide that is crucial for biofilms inside fleas. We also reveal that the Rcs signaling cascade, which represses Hms expression, activates YadE in The ability of to use polysaccharide or YadE protein for cell-cell adhesion may help it produce biofilms in different environments.