Osmotic pressure can regulate matrix gene expression in Bacillus subtilis

Abstract

Many bacteria organize themselves into structurally complex communities known as biofilms in which the cells are held together by an extracellular matrix. In general, the amount of extracellular matrix is related to the robustness of the biofilm. Yet, the specific signals that regulate the synthesis of matrix remain poorly understood. Here we show that the matrix itself can be a cue that regulates the expression of the genes involved in matrix synthesis in Bacillus subtilis. The presence of the exopolysaccharide component of the matrix causes an increase in osmotic pressure that leads to an inhibition of matrix gene expression. We further show that non-specific changes in osmotic pressure also inhibit matrix gene expression and do so by activating the histidine kinase KinD. KinD, in turn, directs the phosphorylation of the master regulatory protein Spo0A, which at high levels represses matrix gene expression. Sensing a physical cue such as osmotic pressure, in addition to chemical cues, could be a strategy to non-specifically coordinate the behavior of cells in communities composed of many different species.

A Combination of Glycerol and Manganese Promotes Biofilm Formation in Bacillus subtilis via Histidine Kinase KinD Signaling

“…For example, Aguilar et al (40) described KinD to be a bifunctional kinase/phosphatase likely sensing the presence of exopolysaccharides and proposed that its chief role is to act as a checkpoint protein linking spore formation to extracellular matrix production during B. subtilis biofilm formation. In another study (20), KinD was proposed to be capable of functioning as an osmosensor, possibly mediated by the transmembrane domain of KinD. KinD also seems to be important in B. subtilis colonization on the plant host by sensing plant-released signals and promoting biofilm formation on the root surface of the plant (19).…”

“…The important role of KinD in biofilm formation and biofilmassociated sporulation has been discussed in several recent studies (19,20,40). For example, Aguilar et al (40) described KinD to be a bifunctional kinase/phosphatase likely sensing the presence of exopolysaccharides and proposed that its chief role is to act as a checkpoint protein linking spore formation to extracellular matrix production during B. subtilis biofilm formation.…”

“…In another recent study (20), the authors suggested that the transmembrane domain of KinD is involved in osmosensing. On the basis of those recent studies, it seems that KinD is likely bifunctional (or multifunctional) in signal sensing.…”

Respiration control of multicellularity in Bacillus subtilis by a complex of the cytochrome chain with a membrane-embedded histidine kinase

“…Evidence indicates that KinD directly or indirectly responds to an unknown small molecule signal released from the roots of tomato plants (which B. subtilis colonizes to form a protective barrier against pathogens) (Chen et al 2012a,b). KinD independently can detect the presence of the extracellular matrix presumably because it is an osmosensor that responds to the osmolarity caused by exopolysaccharide production Rubinstein et al 2012). KinC responds to both membrane damage and potassium ion leakage caused by a self-produced surfactant, surfactin (Lopez et al 2009;Shemesh et al 2010).…”

The Matrix Reloaded: How Sensing the Extracellular Matrix Synchronizes Bacterial Communities

“…While low levels of Spo0AϳP trigger ECM production, high levels trigger sporulation. In this case, the osmotic pressure exerted by both exopolysaccharides and amyloid fibers was shown to be sensed by KinD, as a kinD mutant did not respond to increased osmotic pressure (164). KinD is a membrane histidine kinase that phosphorylates Spo0A and was shown to affect both sporulation and matrix production, with activity redundant with that of KinC (163,165).…”