The two chemotaxis in Caulobacter crescentus operons play different roles in chemotaxis and biofilm regulation

The holdfast polysaccharide adhesin is crucial for irreversible cell adhesion and biofilm formation in Caulobacter crescentus. Holdfast production is tightly controlled via developmental regulators, and environmental and physical signals. Here we identified a novel mechanism of holdfast production regulation that involves chemotaxis proteins. We characterized the two identified chemotaxis operons of C. crescentus and showed that only the previously characterized, major operon is involved in chemotactic response towards different carbon sources. However, both chemotaxis operons encoded in the C. crescentus genome play a role in biofilm formation and holdfast production, by regulating the expression of hfiA, the gene encoding the holdfast inhibitor HfiA. We show that CheA and CheB proteins act in an antagonistic manner: while the two CheA proteins negatively regulate hfiA expression, the CheB proteins are positive regulators, thus providing a modulation of holdfast synthesis and surface attachment. IMPORTANCEChemosensory pathways are major signal transduction mechanisms in bacteria. These systems are involved in chemotaxis and other cell responses to environment conditions, such as production of adhesins that enable irreversible adhesion to a surface and surface colonization. The C. crescentus genome encodes two complete chemotaxis operons. Here we characterized the second, novel chemotaxis-like operon. While only the major chemotaxis operon is involved in chemotaxis, both chemotaxis systems modulate C. crescentus adhesion by controlling expression of the holdfast synthesis inhibitor, HfiA. Thus, we identified a new level in holdfast regulation, providing new insights into the control of adhesin production that leads to the formation of biofilms.