A duo of potassium-responsive histidine kinases govern the multicellular destiny of Bacillus subtilis

GRAU R.; DE OÑA P.; LEÑINI C.; KUIPERS O.

mBio

ASM

Lugar: Washington; Año: 2015 vol. 6 p. 1 - 16

2150-7511

ABSTRACTMulticellular biofilm formation and surface motility are bacterial behaviours considered as mutually exclusive. However, the basic decision to move over or stay attached to a surface is poorly understood. Here, we discover that in Bacillus subtilis, the key root biofilm-controlling transcription factor Spo0A~Pi governs the flagella-independent mechanism of social sliding motility. A Spo0A-deficient strain was totally unable to slide and colonize plant roots evidencing the important role that sliding might play in natural settings. Microarray experiments plus subsequent genetic characterization uncover that the machineries of sliding and biofilm formation, share the same main components (i.e. surfactin, the hydrophobin BslA, exopolysaccharide and de novo-formed fatty acids). Sliding proficiency was transduced by the Spo0A-phosphorelay histidine kinases KinB and KinC. We discover that potassium, a previously known inhibitor of KinC-dependent biofilm formation, is the specific sliding-activating signal through a thus far unnoticed cytosolic domain of KinB, which resembles the selectivity filter sequence of potassium channels. The differential expression of the Spo0A~Pi-reporter abrB gene and the different levels of the constitutively active form of Spo0A, Sad67, in Δspo0A cells grown in optimized media that simultaneously stimulate motile and sessile behaviours, uncover the spatiotemporal response of KinB and KinC to potassium and the gradual increase in Spo0A~Pi that orchestrate the sequential activation of sliding, followed by sessile biofilm formation and finally sporulation in the same population. Overall, these results provide insights into how multicellular behaviours, formerly believed to be antagonistic, are co-ordinately activated in benefit of the bacterium and its interaction with the host.IMPORTANCEAlternation between motile and sessile behaviours is central to bacterial adaptation, survival and colonization. However, how is the collective differentiation to move over or stay attached to a surface controlled? Here, we use the model plant-beneficial bacterium Bacillus subtilis to answer this question. Remarkably, we discover that sessile biofilm formation and social sliding motility share the same structural components and the Spo0A-regulatory network via sensor kinases, KinB and KinC. Potassium, inhibitor of KinC-dependent biofilm formation, triggers sliding via a potassium-perceiving cytosolic domain of KinB that resembles the selectivity filter of potassium channels. The spatiotemporal response of these kinases to variable potassium levels and the gradual increase in Spo0A~Pi levels that orchestrates the activation of sliding before biofilm formation sheds light on how multicellular behaviours, formerly believed to be antagonistic, work together to benefit the population fitness.