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.

Cis- and Trans-Encoded Small Regulatory RNAs in Bacillus subtilis

“…This delays the opuB expression in favor of the expression of opuC , which encodes an alternative but more general osmoprotectant import system. Therefore, S1290 is involved in fine-tuning the salt stress response [ 34 ].…”

Intermolecular Communication in Bacillus subtilis: RNA-RNA, RNA-Protein and Small Protein-Protein Interactions

“…The same holds true for σ B -dependent S1290 that is transiently transcribed in response to salt stress. S1290 acts solely in cis and independent of RNase III on its convergently transcribed target opuB mRNA encoding a choline transporter (Rath et al, 2020). It causes a time-delayed osmotic induction of opuB mRNA, since under acute salt stress, B. subtilis initially relies on the promiscuous OpuC transporter to import pre-formed compatible solutes as proline-or glycine betaine before employing OpuB to import choline that has to be converted into glycine betaine.…”

Salinity of irrigation water selects distinct bacterial communities associated with date palm (Phoenix dactylifera L.) root

“…Pseudomonas , Bacillus and Rhizobium ) are also known to accumulate osmoprotectants (i.e. choline and glycine betaine) 11 – 13 and also elicit antioxidant barricading mechanisms by scavenging reactive oxygen species (ROS) under salinity stress 14 , therefore provide survival advantage to bacteria as well as host. Apart from physiological benefits, the root-associated bacteria (i.e.…”