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Role of the sigmaD-dependent autolysins in Bacillus subtilis population heterogeneity.

ABSTRACT: Exponentially growing populations of Bacillus subtilis contain two morphologically and functionally distinct cell types: motile individuals and nonmotile multicellular chains. Motility differentiation arises because RNA polymerase and the alternative sigma factor sigma(D) activate expression of flagellin in a subpopulation of cells. Here we demonstrate that the peptidoglycan-remodeling autolysins under sigma(D) control, LytC, LytD, and LytF, are expressed in the same subpopulation of cells that complete flagellar synthesis. Morphological heterogeneity is explained by the expression of LytF that is necessary and sufficient for cell separation. Moreover, LytC is required for motility but not at the level of cell separation or flagellum biosynthesis. Rather, LytC appears to be important for flagellar function, and motility was restored to a LytC mutant by mutation of either lonA, encoding the LonA protease, or a gene encoding a previously unannotated swarming motility inhibitor, SmiA. We conclude that heterogeneous activation of sigma(D)-dependent gene expression is sufficient to explain both the morphological heterogeneity and functional heterogeneity present in vegetative B. subtilis populations.

SUBMITTER: Chen R

PROVIDER: S-EPMC2737971 | biostudies-literature | 2009 Sep

REPOSITORIES: biostudies-literature

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Role of the sigmaD-dependent autolysins in Bacillus subtilis population heterogeneity.

Chen Rui R Guttenplan Sarah B SB Blair Kris M KM Kearns Daniel B DB

Journal of bacteriology 20090619 18

Exponentially growing populations of Bacillus subtilis contain two morphologically and functionally distinct cell types: motile individuals and nonmotile multicellular chains. Motility differentiation arises because RNA polymerase and the alternative sigma factor sigma(D) activate expression of flagellin in a subpopulation of cells. Here we demonstrate that the peptidoglycan-remodeling autolysins under sigma(D) control, LytC, LytD, and LytF, are expressed in the same subpopulation of cells that ...[more]

PMID: 19542270

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Project description:We report that the absence of an oxidized guanine (GO) system or the apurinic/apyrimidinic (AP) endonucleases Nfo, ExoA, and Nth promoted stress-associated mutagenesis (SAM) in Bacillus subtilis YB955 (hisC952 metB5 leuC427). Moreover, MutY-promoted SAM was Mfd dependent, suggesting that transcriptional transactions over nonbulky DNA lesions promoted error-prone repair. Here, we inquired whether Mfd and GreA, which control transcription-coupled repair and transcription fidelity, influence the mutagenic events occurring in nutritionally stressed B. subtilis YB955 cells deficient in the GO or AP endonuclease repair proteins. To this end, mfd and greA were disabled in genetic backgrounds defective in the GO and AP endonuclease repair proteins, and the strains were tested for growth-associated and stress-associated mutagenesis. The results revealed that disruption of mfd or greA abrogated the production of stress-associated amino acid revertants in the GO and nfo exoA nth strains, respectively. These results suggest that in nutritionally stressed B. subtilis cells, spontaneous nonbulky DNA lesions are processed in an error-prone manner with the participation of Mfd and GreA. In support of this notion, stationary-phase ΔytkD ΔmutM ΔmutY (referred to here as ΔGO) and Δnfo ΔexoA Δnth (referred to here as ΔAP) cells accumulated 8-oxoguanine (8-OxoG) lesions, which increased significantly following Mfd disruption. In contrast, during exponential growth, disruption of mfd or greA increased the production of His+, Met+, or Leu+ prototrophs in both DNA repair-deficient strains. Thus, in addition to unveiling a role for GreA in mutagenesis, our results suggest that Mfd and GreA promote or prevent mutagenic events driven by spontaneous genetic lesions during the life cycle of B. subtilisIMPORTANCE In this paper, we report that spontaneous genetic lesions of an oxidative nature in growing and nutritionally stressed B. subtilis strain YB955 (hisC952 metB5 leuC427) cells drive Mfd- and GreA-dependent repair transactions. However, whereas Mfd and GreA elicit faithful repair events during growth to maintain genome fidelity, under starving conditions, both factors promote error-prone repair to produce genetic diversity, allowing B. subtilis to escape from growth-limiting conditions.

Dataset Information

Role of the sigmaD-dependent autolysins in Bacillus subtilis population heterogeneity.

Publications

Role of the sigmaD-dependent autolysins in Bacillus subtilis population heterogeneity.

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