Regulation of bacterial surface attachment by a network of sensory transduction proteins

Abstract

AbstractBacteria are often attached to surfaces in natural ecosystems. A surface-associated lifestyle can have advantages, but shifts in the physiochemical state of the environment may result in conditions in which attachment has a negative fitness impact. Therefore, bacterial cells employ numerous mechanisms to control the transition from an unattached to a sessile state. TheCaulobacter crescentusprotein HfiA is a potent developmental inhibitor of the secreted polysaccharide adhesin known as the holdfast, which enables permanent attachment to surfaces. Multiple environmental cues influence expression ofhfiA, but mechanisms ofhfiAregulation remain largely undefined. Through a forward genetic selection, we have discovered a multi-gene network encoding a suite of two-component system (TCS) proteins and transcription factors that coordinately controlhfiAtranscription and surface adhesion. The hybrid HWE-family histidine kinase, SkaH, is central among these regulators and forms heteromeric complexes with the kinases, LovK and SpdS. The response regulator SpdR indirectly inhibitshfiAexpression by activating two XRE-family transcription factors that directly bind thehfiApromoter to repress its transcription. This study provides evidence for a model in which a consortium of environmental sensors and transcriptional regulators integrate environmental cues at thehfiApromoter to control the attachment decision.Author summaryLiving on a surface within a community of cells confers a number of advantages to a bacterium. However, the transition from a free-living state to a surface-attached lifestyle should be tightly regulated to ensure that cells avoid adhering to toxic or resource-limited niches. Many bacteria build adhesive structures at their surfaces that enable attachment. We sought to discover genes that control development of theCaulobacter crescentussurface adhesin known as the holdfast. Our studies uncovered a network of signal transduction proteins that coordinately control the biosynthesis of the holdfast by regulating transcription of the holdfast inhibitor,hfiA. We conclude thatC. crescentususes a multi-component regulatory system to sense and integrate environmental information to determine whether to attach to a surface, or to remain in an unattached state.