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The motility-matrix production switch in Bacillus subtilis-a modeling perspective.

ABSTRACT: Phenotype switching can be triggered by external stimuli and by intrinsic stochasticity. Here, we focus on the motility-matrix production switch in Bacillus subtilis. We use modeling to describe the SinR-SlrR bistable switch and its regulation by SinI and to distinguish different sources of stochasticity. Our simulations indicate that intrinsic fluctuations in the synthesis of SinI are insufficient to drive spontaneous switching and suggest that switching is triggered by upstream noise from the Spo0A phosphorelay. IMPORTANCE The switch from motility to matrix production is the first step toward biofilm formation and, thus, to multicellular behavior in Bacillus subtilis. The transition is governed by a bistable switch based on the interplay of the regulators SinR and SlrR, while SinI transmits upstream signals to that switch. Quantitative modeling can be used to study the switching dynamics. Here, we build such a model step by step to describe the dynamics of the switch and its regulation and to study how spontaneous switching is triggered by upstream noise from the Spo0A phosphorelay.

SUBMITTER: Dannenberg S

PROVIDER: S-EPMC10810213 | biostudies-literature | 2024 Jan

REPOSITORIES: biostudies-literature

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The motility-matrix production switch in <i>Bacillus subtilis</i>-a modeling perspective.

Dannenberg Simon S Penning Jonas J Simm Alexander A Klumpp Stefan S

Journal of bacteriology 20231213 1

Phenotype switching can be triggered by external stimuli and by intrinsic stochasticity. Here, we focus on the motility-matrix production switch in <i>Bacillus subtilis</i>. We use modeling to describe the SinR-SlrR bistable switch and its regulation by SinI and to distinguish different sources of stochasticity. Our simulations indicate that intrinsic fluctuations in the synthesis of SinI are insufficient to drive spontaneous switching and suggest that switching is triggered by upstream noise fr ...[more]

PMID: 38088582

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Project description:While the protein complex responsible for controlling the direction (clockwise [CW] or counterclockwise [CCW]) of flagellar rotation has been fairly well studied in Escherichia coli and Salmonella, less is known about the switch complex in Bacillus subtilis or other Gram-positive species. Two component proteins (FliG and FliM) are shared between E. coli and B. subtilis, but in place of the protein FliN found in E. coli, the B. subtilis complex contains the larger protein FliY. Notably, in B. subtilis the signaling protein CheY-phosphate induces a switch from CW to CCW rotation, opposite to its action in E. coli Here, we have examined the architecture and function of the switch complex in B. subtilis using targeted cross-linking, bacterial two-hybrid protein interaction experiments, and characterization of mutant phenotypes. In major respects, the B. subtilis switch complex appears to be organized similarly to that in E. coli The complex is organized around a ring built from the large middle domain of FliM; this ring supports an array of FliG subunits organized in a similar way to that of E. coli, with the FliG C-terminal domain functioning in the generation of torque via conserved charged residues. Key differences from E. coli involve the middle domain of FliY, which forms an additional, more outboard array, and the C-terminal domains of FliM and FliY, which are organized into both FliY homodimers and FliM heterodimers. Together, the results suggest that the CW and CCW conformational states are similar in the Gram-negative and Gram-positive switches but that CheY-phosphate drives oppositely directed movements in the two cases.IMPORTANCE Flagellar motility plays key roles in the survival of many bacteria and in the harmful action of many pathogens. Bacterial flagella rotate; the direction of flagellar rotation is controlled by a multisubunit protein complex termed the switch complex. This complex has been extensively studied in Gram-negative model species, but little is known about the complex in Bacillus subtilis or other Gram-positive species. Notably, the switch complex in Gram-positive species responds to its effector CheY-phosphate (CheY-P) by switching to CCW rotation, whereas in E. coli or Salmonella CheY-P acts in the opposite way, promoting CW rotation. In the work here, the architecture of the B. subtilis switch complex has been probed using cross-linking, protein interaction measurements, and mutational approaches. The results cast light on the organization of the complex and provide a framework for understanding the mechanism of flagellar direction control in B. subtilis and other Gram-positive species.

Project description:To cope with sudden changes in their environment, bacteria can use a bet-hedging strategy by dividing the population into cells with different properties. This so-called bimodal or bistable cellular differentiation is generally controlled by positive feedback regulation of transcriptional activators. Due to the continuous increase in cell volume, it is difficult for these activators to reach an activation threshold concentration when cells are growing exponentially. This is one reason why bimodal differentiation is primarily observed from the onset of the stationary phase, when exponential growth ceases. An exception is the bimodal induction of motility in Bacillus subtilis, which occurs early during exponential growth. Several mechanisms have been put forward to explain this, including double-negative feedback regulation and the stability of the mRNA molecules involved. In this study, we used fluorescence-assisted cell sorting (FACS) to compare the transcriptomes of motile and nonmotile cells and noted that expression of ribosomal genes is lower in motile cells. This was confirmed using an unstable green fluorescent protein (GFP) reporter fused to the strong ribosomal rpsD promoter. We propose that the reduction in ribosomal gene expression in motile cells is the result of a diversion of cellular resources to the synthesis of the chemotaxis and motility systems. In agreement with this, single-cell microscopic analysis showed that motile cells are slightly shorter than nonmotile cells, an indication of slower growth. We speculate that this growth rate reduction can contribute to the bimodal induction of motility during exponential growth. IMPORTANCE To cope with sudden environmental changes, bacteria can use a bet-hedging strategy and generate different types of cells within a population-so-called bimodal differentiation. For example, a Bacillus subtilis culture can contain both motile and nonmotile cells. In this study, we compared the gene expression between motile and nonmotile cells. It appeared that motile cells express fewer ribosomes. To confirm this, we constructed a ribosomal promoter fusion that enabled us to measure expression of this promoter in individual cells. This reporter fusion confirmed our initial finding. The reallocation of cellular resources from ribosome synthesis toward synthesis of the motility apparatus results in a reduction in growth. Interestingly, this growth reduction has been shown to stimulate bimodal differentiation.

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The motility-matrix production switch in Bacillus subtilis-a modeling perspective.

Publications

The motility-matrix production switch in <i>Bacillus subtilis</i>-a modeling perspective.

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