Small Regulatory RNA-Induced Growth Rate Heterogeneity of Bacillus subtilis

Mars, Ruben A. T.; Nicolas, Pierre; Ciccolini, Mariano; Reilman, Ewoud; Reder, Alexander; Schaffer, Marc; Mäder, Ulrike; Völker, Uwe; Dijl, Jan Maarten van; Denham, Emma L.

doi:10.1371/journal.pgen.1005046

Cited by 44 publications

(44 citation statements)

References 65 publications

(107 reference statements)

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“…Recently, RnaC/S1022 was shown to modulate the cellular levels of the important transcriptional regulator AbrB via a direct sRNA-mRNA interaction (24). Interestingly, this repressive sRNA regulation of AbrB results in an increased cell-to-cell variation of the AbrB levels, as was demonstrated with green fluorescent protein (GFP)-tagged AbrB.…”

Section: Independently Expressed Small Rnas and Rna Antitoxinsmentioning

confidence: 92%

“…Interestingly, this repressive sRNA regulation of AbrB results in an increased cell-to-cell variation of the AbrB levels, as was demonstrated with green fluorescent protein (GFP)-tagged AbrB. Linked to AbrB being essential for B. subtilis growth in the employed M9 minimal medium, the RnaC/S1022-induced diversity in the cellular AbrB protein levels leads to heterogeneity in the growth rates of different cells within one population during the exponential phase (24). It was proposed that this sRNA-induced growth rate heterogeneity could reflect a bet-hedging strategy for enhanced survival under unfavorable conditions.…”

Section: Independently Expressed Small Rnas and Rna Antitoxinsmentioning

confidence: 93%

“…Despite this, genes encoding Hfq homologues are found only in approximately half of the currently sequenced genomes (22), indicating that there may be alternative ways of mediating RNA regulation. This view is underscored by studies on B. subtilis, which contains an Hfq homologue (previously named YmaH) that is dispensable for the sRNA-mRNA interactions reported in this organism so far (23,24). In addition, recent studies on the influence of B. subtilis Hfq at the transcriptome level have shown that while Hfq has some influence on RNA regulatory processes, this was not to the extent that has been reported for other species (23,132).…”

Section: Rna Chaperones In B Subtilismentioning

confidence: 95%

“…This might be linked to the reported minor importance of the RNA chaperone Hfq to RNA regulation in most Gram-positive bacteria, and B. subtilis in particular. In contrast, the critical role of Hfq in Gram-negative bacteria greatly facilitated the many studies on RNA regulation in the respective species (22)(23)(24). To bridge current knowledge gaps, we now provide a global description of all identified regulatory RNAs of B. subtilis.…”

Section: Scope Of the Reviewmentioning

confidence: 99%

“…RnaC/S1022 was first identified in a microarray screen of B. subtilis intergenic regions, and its expression was found to be completely dependent on the sigma factor SigD during the exponential growth phase on LB medium (24,109). Recently, RnaC/S1022 was shown to modulate the cellular levels of the important transcriptional regulator AbrB via a direct sRNA-mRNA interaction (24).…”

Section: Independently Expressed Small Rnas and Rna Antitoxinsmentioning

confidence: 99%

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Regulatory RNAs in Bacillus subtilis: a Gram-Positive Perspective on Bacterial RNA-Mediated Regulation of Gene Expression

Mars

Nicolas

Denham

et al. 2016

Microbiol Mol Biol Rev

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SUMMARY Bacteria can employ widely diverse RNA molecules to regulate their gene expression. Such molecules include trans -acting small regulatory RNAs, antisense RNAs, and a variety of transcriptional attenuation mechanisms in the 5′ untranslated region. Thus far, most regulatory RNA research has focused on Gram-negative bacteria, such as Escherichia coli and Salmonella . Hence, there is uncertainty about whether the resulting insights can be extrapolated directly to other bacteria, such as the Gram-positive soil bacterium Bacillus subtilis . A recent study identified 1,583 putative regulatory RNAs in B. subtilis , whose expression was assessed across 104 conditions. Here, we review the current understanding of RNA-based regulation in B. subtilis , and we categorize the newly identified putative regulatory RNAs on the basis of their conservation in other bacilli and the stability of their predicted secondary structures. Our present evaluation of the publicly available data indicates that RNA-mediated gene regulation in B. subtilis mostly involves elements at the 5′ ends of mRNA molecules. These can include 5′ secondary structure elements and metabolite-, tRNA-, or protein-binding sites. Importantly, sense-independent segments are identified as the most conserved and structured potential regulatory RNAs in B. subtilis . Altogether, the present survey provides many leads for the identification of new regulatory RNA functions in B. subtilis .

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Section: Independently Expressed Small Rnas and Rna Antitoxinsmentioning

confidence: 92%

Section: Independently Expressed Small Rnas and Rna Antitoxinsmentioning

confidence: 93%

Section: Rna Chaperones In B Subtilismentioning

confidence: 95%

Section: Scope Of the Reviewmentioning

confidence: 99%

Section: Independently Expressed Small Rnas and Rna Antitoxinsmentioning

confidence: 99%

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Regulatory RNAs in Bacillus subtilis: a Gram-Positive Perspective on Bacterial RNA-Mediated Regulation of Gene Expression

Mars

Nicolas

Denham

et al. 2016

Microbiol Mol Biol Rev

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RNA sequencing reveals small RNAs in Bacillus pumilus under different growth phases of the protease fermentation process

Zhao

et al. 2019

Appl Microbiol Biotechnol

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Transcription termination factor Rho and microbial phenotypic heterogeneity

Bidnenko

2017

Curr Genet

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Populations of genetically identical microorganisms exhibit high degree of cell-to-cell phenotypic diversity even when grown in uniform environmental conditions. Heterogeneity is a genetically determined trait, which ensures bacterial adaptation and survival in the ever changing environmental conditions. Fluctuations in gene expression (noise) at the level of transcription initiation largely contribute to cell-to-cell variability within population. Not surprisingly, the analyses of the mechanisms driving phenotypic heterogeneity are mainly focused on the activity of promoters and transcriptional factors. Less attention is currently given to a role of intrinsic and factor-dependent transcription terminators. Here, we discuss recent advances in understanding the regulatory role of the multi-functional transcription termination factor Rho, the major inhibitor of pervasive transcription in bacteria and the emerging global regulator of gene expression. We propose that termination activity of Rho might be among the mechanisms by which cells manage the intensity of transcriptional noise, thus affecting population heterogeneity.

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Small Regulatory RNA-Induced Growth Rate Heterogeneity of Bacillus subtilis

Cited by 44 publications

References 65 publications

Regulatory RNAs in Bacillus subtilis: a Gram-Positive Perspective on Bacterial RNA-Mediated Regulation of Gene Expression

Regulatory RNAs in Bacillus subtilis: a Gram-Positive Perspective on Bacterial RNA-Mediated Regulation of Gene Expression

RNA sequencing reveals small RNAs in Bacillus pumilus under different growth phases of the protease fermentation process

Transcription termination factor Rho and microbial phenotypic heterogeneity

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