A role for the essential YycG sensor histidine kinase in sensing cell division

Fukushima, Tatsuya; Furihata, Isako; Emmins, Robyn; Daniel, Richard A.; Hoch, James A.; Szurmant, Hendrik

doi:10.1111/j.1365-2958.2010.07464.x

Cited by 61 publications

(71 citation statements)

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“…1) proposes that the WalRK TCS senses cell growth through septal location of WalK and is activated by a signal emanating from the divisome (Fukushima et al, 2008(Fukushima et al, , 2011. WalR-P activates expression of autolysins (CwlO, YocH and LytE), cell-wall-associated (YdjM) and cell division (FtsZ) proteins while repressing autolysin-modulating (YjeA) and -inhibiting (IseA) activities thereby promoting cell wall synthesis during cell elongation (Bisicchia et al, 2007;Fukushima et al, 2008Fukushima et al, , 2011. During phosphate limitation, the WalK signal is lowered or absent due to reduced growth rate, but peptidoglycan synthesis is still required (Bisicchia et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Cell envelope gene expression in phosphate-limited Bacillus subtilis cells

et al. 2011

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The high phosphate content of Bacillus subtilis cell walls dictates that cell wall metabolism is an important feature of the PhoPR-mediated phosphate limitation response. Here we report the expression profiles of cell-envelope-associated and PhoPR regulon genes, determined by live cell array and transcriptome analysis, in exponentially growing and phosphate-limited B. subtilis cells. Control by the WalRK two-component system confers a unique expression profile and high level of promoter activity on the genes of its regulon with yocH and cwlO expression differing both qualitatively and quantitatively from all other autolysin-encoding genes examined. The activity of the PhoPR two-component system is restricted to the phosphate-limited state, being rapidly induced in response to the cognate stimulus, and can be sustained for an extended phosphate limitation period. Constituent promoters of the PhoPR regulon show heterogeneous induction profiles and very high promoter activities. Phosphate-limited cells also show elevated expression of the actin-like protein MreBH and reduced expression of the WapA cell wall protein and WprA cell wall protease indicating that cell wall metabolism in this state is distinct from that of exponentially growing and stationary-phase cells. The PhoPR response is very rapidly deactivated upon removal of the phosphate limitation stimulus with concomitant increased expression of cell wall metabolic genes. Moreover expression of genes encoding enzymes involved in sulphur metabolism is significantly altered in the phosphate-limited state with distinct perturbations being observed in wild-type 168 and AH024 (DphoPR) cells.

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Section: Introductionmentioning

confidence: 99%

Cell envelope gene expression in phosphate-limited Bacillus subtilis cells

et al. 2011

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“…YycG kinase, like MtrB, associates with the septa, and its septal association is essential for its activation and for controlling the expression of several genes involved in cell wall metabolism and turnover (34,35). Pertinent to this study is the observation that the YycG kinase interacts with PbpB (FtsI) and with other proteins, such as FtsL and DivIB (34). These studies also showed that the septal localization of YycG is not affected by the depletion of DivIB and FtsL and that studies with PbpB depletion are not conclusive.…”

Section: Discussionmentioning

confidence: 99%

Mycobacterium tuberculosis MtrB Sensor Kinase Interactions with FtsI and Wag31 Proteins Reveal a Role for MtrB Distinct from That Regulating MtrA Activities

et al. 2014

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The septal association of Mycobacterium tuberculosis MtrB, the kinase partner of the MtrAB two-component signal transduction system, is necessary for the optimal expression of the MtrA regulon targets, including ripA, fbpB, and ftsI, which are involved in cell division and cell wall synthesis. Here, we show that MtrB, irrespective of its phosphorylation status, interacts with Wag31, whereas only phosphorylation-competent MtrB interacts with FtsI. We provide evidence that FtsI depletion compromises the MtrB septal assembly and MtrA regulon expression; likewise, the absence of MtrB compromises FtsI localization and, possibly, FtsI activity. We conclude from these results that FtsI and MtrB are codependent for their activities and that FtsI functions as a positive modulator of MtrB activation and MtrA regulon expression. In contrast to FtsI, Wag31 depletion does not affect MtrB septal assembly and MtrA regulon expression, whereas the loss of MtrB increased Wag31 localization and the levels of PknA/PknB (PknA/B) serine-threonine protein kinase-mediated Wag31 phosphorylation. Interestingly, we found that FtsI decreased levels of phosphorylated Wag31 (Wag31ϳP) and that MtrB interacted with PknA/B. Overall, our results indicate that MtrB interactions with FtsI, Wag31, and PknA/B are required for its optimal localization, MtrA regulon expression, and phosphorylation of Wag31. Our results emphasize a new role for MtrB in cell division and cell wall synthesis distinct from that regulating the MtrA phosphorylation activities.

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“…What domain of YycG kinase was interacting with the septum? Tetsuya was able to show that the cytoplasmic PAS domain of this multiple-domain transmembrane kinase was a determining factor translocating the kinase to the division septum (19).…”

Section: An Essential Two-component System Connecting Cell Wall Growtmentioning

confidence: 99%

A Life inBacillus subtilisSignal Transduction

Hoch

2017

Annu. Rev. Microbiol.

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This is a tale of how technology drove the discovery of the molecular basis for signal transduction in the initiation of sporulation in Bacillus subtilis and in bacterial two-component systems. It progresses from genetics to cloning and sequencing to biochemistry to structural biology to an understanding of how proteins evolve interaction specificity and to identification of interaction surfaces by statistical physics. This is about how the people in my laboratory accomplished this feat; without them little would have been done.

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A role for the essential YycG sensor histidine kinase in sensing cell division

Cited by 61 publications

References 50 publications

Cell envelope gene expression in phosphate-limited Bacillus subtilis cells

Cell envelope gene expression in phosphate-limited Bacillus subtilis cells

Mycobacterium tuberculosis MtrB Sensor Kinase Interactions with FtsI and Wag31 Proteins Reveal a Role for MtrB Distinct from That Regulating MtrA Activities

A Life inBacillus subtilisSignal Transduction

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