Cell cycle progression and stalked cell morphogenesis in Caulobacter crescentus are regulated independently by the flagellum

Abstract

Bacteria colonize surfaces and form biofilms to survive in stressful environmental conditions. Many bacteria use an appendage called the flagellum to sense surface contact, and responding to these mechanical cues triggers rapid physiological changes to promote downstream attachment. Bacteria are known to secrete adhesins and alter their motility behavior to facilitate surface colonization, but these changes alone are insufficient to explain the breadth of adaptations observed in surface-attached cells. Disrupting flagellar assembly in the bacterium Caulobacter crescentus constitutively activates the surface sensing pathway, and this gain-of-function phenotype was previously used to identify a suite of flagellar signaling suppressor (fss) genes that promotes surface adhesion downstream of the flagellum. We show herein that a subset of fss genes also regulates the C. crescentus developmental program. Live-cell microscopy analysis of fss mutants identified independent sub-pathways that target stalked cell morphogenesis and cell cycle progression. We identify the predicted chemotaxis genes fssD and fssE as novel regulators of stalked cell morphogenesis and show that these genes act to stimulate the diguanylate cyclase PleD in flagellar assembly mutants. A separate pathway that includes the stator protein MotB and the recently characterized dNTPase FssC regulates entry into S phase downstream of the flagellum. We show that motB regulates cell cycle progression specifically in response to surface cues, and that stator-dependent cell cycle control occurs independently of c-di-GMP and CtrA. This work clarifies the downstream targets of the surface sensing network and establishes a comprehensive model for how surface sensing influences the C. crescentus developmental program.