Different roles for KinA, KinB, and KinC in the initiation of sporulation in Bacillus subtilis

Abstract

Activation (phosphorylation) of the transcription factor encoded by spo0A is essential for the initiation of sporulation in Bacillus subtilis. At least three histidine protein kinases are involved in the phosphorylation of Spo0A. Under some growth conditions, KinA was the primary kinase, but under other conditions, KinB had the more critical role. KinC was required for the initial activation of Spo0A, even in the presence of KinA and KinB.Under appropriate conditions, cells of the gram-positive soil bacterium Bacillus subtilis differentiate to form dormant heatresistant endospores. One of the key factors determining whether cells initiate sporulation is the accumulation of the active phosphorylated form of the transcription factor encoded by spo0A (reviewed in reference 7). Spo0A belongs to the response regulator family of transcription factors (1, 20) which usually receive phosphate on an aspartate residue from histidine protein kinases known as sensor kinases (1,20). The histidine protein kinases autophosphorylate on a histidine residue and then serve as a phosphate donor to a cognate response regulator. Unlike most response regulators, Spo0A does not receive phosphate directly from a histidine protein kinase. Rather, phosphorylation of Spo0A requires the transfer of phosphate through the phosphorelay (5). The sporulation kinases first serve as phosphate donors to the response regulator encoded by spo0F. Phosphate is then transferred from Spo0F to Spo0B and finally to Spo0A (5, 7). The physiological function of the phosphorelay seems to be to integrate the many signals that regulate the initiation of sporulation (8, 10-13) and to generate a threshold concentration of Spo0AϳP necessary for the initiation of sporulation (6).Spo0AϳP is a transcriptional activator and repressor, depending on the location of the target binding site. Spo0AϳP represses transcription of abrB (22, 27) and activates transcription of several sporulation genes, including spoIIA (28), spoIIE (32), and spoIIG (3, 4). The abrB gene product is a transcriptional repressor, and repression of abrB by Spo0AϳP causes activation of genes that are normally repressed by AbrB (31,34). Less Spo0AϳP is needed for repression of abrB than for activation of the spoII genes, since several mutations that decrease activation of Spo0A have little or no effect on abrB expression while causing a decrease in expression of spoII genes (6,19,21,26,29).Three histidine protein kinases are involved in the initiation of sporulation: KinA (2, 21), KinB (29), and KinC (15,16). Under most sporulation conditions tested, kinA null mutations cause a small reduction in the sporulation frequency while null mutations in either kinB or kinC cause little or no decrease in sporulation frequency (15,16,29). The experiments described

Characterization of Sporulation Histidine Kinases ofBacillus anthracis

“…The ultimate goal of the phosphorelay is to activate by phosphorylation the Spo0A transcription factor, which represses certain genes and promotes the transcription of a large number of genes for stationary-phase functions as well as sporulation (16,23). The signals that initiate the phosphorelay reactions are recognized and interpreted by several sensor histidine kinases (10,11,13,14). While the nature of these signals in Bacillus subtilis and other Bacillus species remains a mystery, the target of their activation is the Spo0F response regulator, to which they transfer a phosphoryl group.…”

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

“…Five histidine kinases (KinA-E) feed phosphoryl groups into the relay, but only four (KinA, KinB, KinC, and KinD) contribute significantly to biofilm formation, and only two (KinA and KinB) play an important role in spore formation (Burbulys et al 1991;LeDeaux et al 1995;Tzeng et al 1998;McLoon et al 2011). 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).…”

Proteome-wide analysis of the functional roles of bacilysin biosynthesis in Bacillus subtilis

“…The low-threshold Spo0A-regulated gene abrB has been reported to be expressed at submaximal levels during logarithmical growth of wildtype cells, compared with the levels reached in strains with an inactivated phosphorelay (Perego et al, 1988;Trach and Hoch, 1993). Submaximal levels of abrB expression during logarithmical growth were also observed in kinA, kinB or kinE mutant strains, but the expression levels were higher in kinC and kinD mutant strains, and maximum abrB expression levels were observed in the absence of both KinC and KinD (Trach and Hoch, 1993;LeDeaux et al, 1995;Jiang et al, 2000). From these results, it was inferred that KinC and KinD would be responsible for generating Spo0A~P to levels causing partial repression of abrB transcription during logarithmical growth (Castillo-Llorente et al, 2008).…”