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- Title
Termination factor Rho mediates transcriptional reprogramming of Bacillus subtilis stationary phase.
- Authors
Bidnenko, Vladimir; Nicolas, Pierre; Guérin, Cyprien; Dérozier, Sandra; Chastanet, Arnaud; Dairou, Julien; Redko-Hamel, Yulia; Jules, Matthieu; Bidnenko, Elena
- Abstract
Transcription termination factor Rho is known for its ubiquitous role in suppression of pervasive, mostly antisense, transcription. In the model Gram-positive bacterium Bacillus subtilis, de-repression of pervasive transcription by inactivation of rho revealed the role of Rho in the regulation of post-exponential differentiation programs. To identify other aspects of the regulatory role of Rho during adaptation to starvation, we have constructed a B. subtilis strain (Rho+) that expresses rho at a relatively stable high level in order to compensate for its decrease in the wild-type cells entering stationary phase. The RNAseq analysis of Rho+, WT and Δrho strains (expression profiles can be visualized at http://genoscapist.migale.inrae.fr/seb%5frho/) shows that Rho over-production enhances the termination efficiency of Rho-sensitive terminators, thus reducing transcriptional read-through and antisense transcription genome-wide. Moreover, the Rho+ strain exhibits global alterations of sense transcription with the most significant changes observed for the AbrB, CodY, and stringent response regulons, forming the pathways governing the transition to stationary phase. Subsequent physiological analyses demonstrated that maintaining rho expression at a stable elevated level modifies stationary phase-specific physiology of B. subtilis cells, weakens stringent response, and thereby negatively affects the cellular adaptation to nutrient limitations and other stresses, and blocks the development of genetic competence and sporulation. These results highlight the Rho-specific termination of transcription as a novel element controlling stationary phase. The release of this control by decreasing Rho levels during the transition to stationary phase appears crucial for the functionality of complex gene networks ensuring B. subtilis survival in stationary phase. Author summary: The Gram-positive soil-dwelling bacterium Bacillus subtilis is well known for its ability to adapt to changing and often unfavorable environmental conditions. To improve the chances of survival, B. subtilis employs various strategies that range from global modifications of cellular metabolism that are characteristic to stationary phase and allowing starvation resistance, to alternative programs of cellular differentiation, including the formation of dormant and highly resistant spores as an ultimate survival option. All these processes rely on the functioning of complex and interconnected gene networks, which are controlled by several well-known global transcription regulators acting at the level of transcription initiation. Here we show that the termination factor Rho, responsible for the main factor-dependent pathway of transcription termination and the major inhibitor of antisense transcription in bacteria, is intricately involved in the control of adaptation of B. subtilis cells to stationary phase. Notably, maintaining Rho at a constant level during exponential growth and stationary phase triggers transcriptional reprogramming and modifies the stationary-phase physiology of B. subtilis cells to such an extent that it negatively affects cellular adaptation to nutrient limitation and cell-fate decision-making. Therefore, the transcription termination factor Rho imposes a new layer of control over stationary phase and adaptive strategies in B. subtilis.
- Subjects
RHO factor; BACILLUS (Bacteria); GENE regulatory networks; BACILLUS subtilis; GENE expression; PHASE transitions
- Publication
PLoS Genetics, 2023, Vol 18, Issue 2, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010618