Dataset Information

Management of Osmoprotectant Uptake Hierarchy in Bacillus subtilis via a SigB-Dependent Antisense RNA.

ABSTRACT: Under hyperosmotic conditions, bacteria accumulate compatible solutes through synthesis or import. Bacillus subtilis imports a large set of osmostress protectants via five osmotically controlled transport systems (OpuA to OpuE). Biosynthesis of the particularly effective osmoprotectant glycine betaine requires the exogenous supply of choline. While OpuB is rather specific for choline, OpuC imports a broad spectrum of compatible solutes, including choline and glycine betaine. One previously mapped antisense RNA of B. subtilis, S1290, exhibits strong and transient expression in response to a suddenly imposed salt stress. It covers the coding region of the opuB operon and is expressed from a strictly SigB-dependent promoter. By inactivation of this promoter and analysis of opuB and opuC transcript levels, we discovered a time-delayed osmotic induction of opuB that crucially depends on the S1290 antisense RNA and on the degree of the imposed osmotic stress. Time-delayed osmotic induction of opuB is apparently caused by transcriptional interference of RNA-polymerase complexes driving synthesis of the converging opuB and S1290 mRNAs. When our data are viewed in an ecophysiological framework, it appears that during the early adjustment phase of B. subtilis to acute osmotic stress, the cell prefers to initially rely on the transport activity of the promiscuous OpuC system and only subsequently fully induces opuB. Our data also reveal an integration of osmostress-specific adjustment systems with the SigB-controlled general stress response at a deeper level than previously appreciated.

SUBMITTER: Rath H

PROVIDER: S-EPMC7186363 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Publications

Management of Osmoprotectant Uptake Hierarchy in <i>Bacillus subtilis</i> via a SigB-Dependent Antisense RNA.

Rath Hermann H Reder Alexander A Hoffmann Tamara T Hammer Elke E Seubert Andreas A Bremer Erhard E Völker Uwe U Mäder Ulrike U

Frontiers in microbiology 20200421

Under hyperosmotic conditions, bacteria accumulate compatible solutes through synthesis or import. <i>Bacillus subtilis</i> imports a large set of osmostress protectants via five osmotically controlled transport systems (OpuA to OpuE). Biosynthesis of the particularly effective osmoprotectant glycine betaine requires the exogenous supply of choline. While OpuB is rather specific for choline, OpuC imports a broad spectrum of compatible solutes, including choline and glycine betaine. One previousl ...[more]

PMID: 32373088

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Project description:The sigma(B)-dependent general stress regulon of Bacillus subtilis comprises more than 150 members. Induction of this regulon by imposition of environmental or metabolic stress confers multiple, nonspecific, and preemptive stress resistance to nongrowing, nonsporulated cells of B. subtilis. In this study we performed a regulon-wide phenotypic screening analysis to determine the stress sensitivity profiles of 94 mutants defective in candidate members of the general stress regulon that were previously identified in our transcriptional profiling study of the general stress response of B. subtilis. The phenotypic screening analysis included analysis of adaptation to a growth-inhibiting concentration of ethanol (10%, vol/vol) or NaCl (10%, wt/vol), severe heat shock (54 degrees C), and low temperature (survival at 4 degrees C and growth at 12.5 degrees C). Surprisingly, 85% of the mutants tested displayed increased sensitivity at an alpha confidence level of < or =0.01 to at least one of the four stresses tested, and 62% still exhibited increased sensitivity at an alpha of < or =0.001. In essence, we were able to assign 63 genes (28 genes with an alpha of < or =0.001) to survival after ethanol shock, 37 genes (28 genes with an alpha of < or =0.001) to protection from NaCl shock, 34 genes (24 genes with an alpha of < or =0.001) to survival at 4 degrees C, and 10 genes (3 genes with an alpha of < or =0.001) to management of severe heat shock. Interestingly, there was a substantial overlap between the genes necessary for survival during ethanol shock and the genes necessary for survival at 4 degrees C, and there was also an overlap between genes required for survival during ethanol shock and genes required for survival during NaCl shock. Our data provide evidence for the importance of the sigma(B) regulon at low temperatures, not only for growth but also for survival. Moreover, the data imply that a secondary oxidative stress seems to be a common component of the severe stresses tested.

Project description:Bacterial biofilms are important in natural settings, biotechnology, and medicine. However, regulation of biofilm development and its persistence in different niches is complex and only partially understood. One key step during the biofilm life cycle is dispersal, when motile cells abandon the mature biofilm to spread out and colonize new niches. Here, we show that in the model bacterium Bacillus subtilis the general stress transcription factor SigB is essential for halting detrimental overgrowth of mature biofilm and for triggering dispersal when nutrients become limited. Specifically, SigB-deficient biofilms were larger than wild-type biofilms but exhibited accelerated cell death, significantly greater sensitivity to different stresses, and reduced dispersal. Interestingly, the signal detected by SigB to limit biofilm growth was transduced through the RsbP-dependent metabolic arm of the SigB regulatory cascade, which in turn positively controlled expression of SinR, the master regulator of biofilm formation and cell motility. This novel SigB-SinR regulatory circuit might be important in controlling the fitness of biofilms (either beneficial or harmful) in diverse environments.IMPORTANCE Biofilms are crucial for bacterial survival, adaptation, and dissemination in natural, industrial, and medical systems. Sessile cells embedded in the self-produced extracellular matrix of the biofilm benefit from a division of labor and are protected from environmental insults. However, as the biofilm ages, cells become stressed because of overcrowding, starvation, and accumulation of waste products. How does the sessile biofilm community sense and respond to stressful conditions? Here, we show that in Bacillus subtilis, the transcription factors SigB and SinR control whether cells remain in or leave a biofilm when metabolic conditions become unfavorable. This novel SigB-SinR regulatory circuit might be important for controlling the fitness of biofilms (either beneficial or harmful) in diverse environments.

Dataset Information

Management of Osmoprotectant Uptake Hierarchy in Bacillus subtilis via a SigB-Dependent Antisense RNA.

Publications

Management of Osmoprotectant Uptake Hierarchy in <i>Bacillus subtilis</i> via a SigB-Dependent Antisense RNA.

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