A flagellar accessory protein links chemotaxis to surface sensing

Abstract

AbstractBacteria find suitable locations for colonization by sensing and responding to surfaces. Complex signaling repertoires control surface colonization, and surface contact sensing by the flagellum plays a central role in activating colonization programs.Caulobacter crescentusadheres to surfaces using a polysaccharide adhesin called the holdfast. InC. crescentus, disruption of the flagellum through interactions with a surface or mutation of flagellar genes increases holdfast production. Our group previously identified severalC. crescentusgenes involved in flagellar surface sensing. One of these, calledfssF, codes for a protein with homology to the flagellar C-ring protein FliN. We show here that a fluorescently tagged FssF protein localizes to the flagellated pole of the cell and requires all components of the flagellar C-ring for proper localization, supporting the model that FssF associates with the C-ring. DeletingfssFresults in a severe motility defect that we show is due to a disruption of chemotaxis. Epistasis experiments demonstrate thatfssFpromotes adhesion through a stator-dependent pathway when late-stage flagellar mutants are disrupted. Separately, we find that disruption of chemotaxis through deletion offssFor other chemotaxis genes results in a hyperadhesion phenotype. Key genes in the surface sensing network (pleD,motB, anddgcB) contribute to both ΔflgH-dependent and ΔfssF-dependent hyperadhesion, but these genes affect adhesion differently in the two hyperadhesive backgrounds. Our results support a model in which the stator subunits of the flagella incorporate both mechanical and chemical signals to regulate adhesion.ImportanceBiofilms pose a threat in clinical and industrial settings. Surface sensing is an early step in biofilm formation. Studying surface sensing can help develop strategies for combating harmful biofilms. Here, we use the freshwater bacteriumCaulobacter crescentusto study surface sensing. We characterize a previously unstudied gene,fssF, and find that it localizes to the cell pole in the presence of three proteins that make up a component of the flagellum called the C-ring. Additionally, we find thatfssFis required for chemotaxis but dispensable for swimming motility. Lastly, our results show that mutatingfssFand other genes required for chemotaxis causes a hyperadhesive phenotype. We propose that surface sensing requires chemotaxis for a robust response to a surface.