Osmotic control of opuA expression in Bacillus subtilis and its modulation in response to intracellular glycine betaine and proline pools.
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Glycine betaine is an effective osmoprotectant for Bacillus subtilis. Its import into osmotically stressed cells led to the buildup of large pools, whose size was sensitively determined by the degree of the osmotic stress imposed. The amassing of glycine betaine caused repression of the formation of an osmostress-adaptive pool of proline, the only osmoprotectant that B. subtilis can synthesize de novo. The ABC transporter OpuA is the main glycine betaine uptake system of B. subtilis. Expression of opuA was upregulated in response to both sudden and sustained increases in the external osmolarity. Nonionic osmolytes exerted a stronger inducing effect on transcription than ionic osmolytes, and this was reflected in the development of corresponding OpuA-mediated glycine betaine pools. Primer extension analysis and site-directed mutagenesis pinpointed the osmotically controlled opuA promoter. Deviations from the consensus sequence of SigA-type promoters serve to keep the transcriptional activity of the opuA promoter low in the absence of osmotic stress. opuA expression was downregulated in a finely tuned manner in response to increases in the intracellular glycine betaine pool, regardless of whether this osmoprotectant was imported or was newly synthesized from choline. Such an effect was also exerted by carnitine, an effective osmoprotectant for B. subtilis that is not a substrate for the OpuA transporter. opuA expression was upregulated in a B. subtilis mutant that was unable to synthesize proline in response to osmotic stress. Collectively, our data suggest that the intracellular solute pool is a key determinant for the osmotic control of opuA expression.
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Osmotic induction of the opuB and opuC promoters requires the formation of an increased osmotic gradient across the cytoplasmic membrane.
“As observed with other osmotically regulated B. subtilis genes (Hoffmann et al., 2013), osmotic induction of the opuB and opuC promoters requires the formation of an increased osmotic gradient across the cytoplasmic membrane.”
From Two MarR-Type Repressors Balance Precursor Uptake and Glycine Betaine Synthesis in Bacillus subtilis to Provide Cytoprotection Against Sustained Osmotic Stress (2020) · cites this paper as Hoffmann et al., 2013
The glycine betaine pool attained via import by a B. subtilis wild-type cell is linearly dependent on the degree of imposed osmotic stress.
“The glycine betaine pool attained via import of a B. subtilis wild-type cell is linearly dependent on the degree of the imposed osmotic stress (Hoffmann et al., 2013).”
From Two MarR-Type Repressors Balance Precursor Uptake and Glycine Betaine Synthesis in Bacillus subtilis to Provide Cytoprotection Against Sustained Osmotic Stress (2020) · cites this paper as Hoffmann et al., 2013
Salinities higher than 0.5 M NaCl in minimal medium with glucose cause a strong growth rate decrease of B. subtilis cultures; doubling times increase from 1 h to nearly 5 h in SMM with 1.2 M NaCl.
“Salinities higher than 0.5 M NaCl added to a minimal medium with glucose as the sole carbon and energy source cause a strong growth rate decrease of B. subtilis cultures; doubling times increase from 1 h to nearly 5 h (in SMM with added 1.2 M NaCl) (Boch et al., 1994; Hoffmann et al., 2013).”
From Two MarR-Type Repressors Balance Precursor Uptake and Glycine Betaine Synthesis in Bacillus subtilis to Provide Cytoprotection Against Sustained Osmotic Stress (2020) · cites this paper as Hoffmann et al., 2013
To maintain a physiologically adequate osmoprotective glycine betaine pool, uptake rates for glycine betaine and its biosynthetic precursor choline must be adjusted to both the imposed osmotic stress and the dynamic increase in cell volume prior to division.
“However, in order to maintain a physiologically adequate osmoprotective glycine betaine pool (and for that matter of other compatible solutes as well), the uptake rates for glycine betaine and its biosynthetic precursor choline must be adjusted to both the level of the imposed osmotic stress (Hoffmann et al., 2013) but concomitantly also to the dynamic increase in cell volume prior to division of”
From Two MarR-Type Repressors Balance Precursor Uptake and Glycine Betaine Synthesis in Bacillus subtilis to Provide Cytoprotection Against Sustained Osmotic Stress (2020) · cites this paper as Hoffmann et al., 2013
The B. subtilis strain TMB118, lacking OpuA, OpuB, OpuC, and OpuD transporters, cannot import glycine betaine or choline.
“The B. subtilis strain TMB118, which lacks the OpuA, OpuB, OpuC, and OpuD transporters (Teichmann et al., 2017; Supplementary Table S2), was used as a negative control to assess the true import of glycine betaine and choline.”
From Two MarR-Type Repressors Balance Precursor Uptake and Glycine Betaine Synthesis in Bacillus subtilis to Provide Cytoprotection Against Sustained Osmotic Stress (2020) · cites this paper as Hoffmann et al., 2013
The observed glycine betaine and choline values in TMB118 extracts represent incomplete removal of these compounds from outside intact cells during harvesting.
“These values represent the incomplete removal of glycine betaine or choline from the outside of intact cells during harvesting of the samples, since the mutant strain TMB118 cannot import glycine betaine or choline (Hoffmann et al., 2013).”
From Two MarR-Type Repressors Balance Precursor Uptake and Glycine Betaine Synthesis in Bacillus subtilis to Provide Cytoprotection Against Sustained Osmotic Stress (2020) · cites this paper as Hoffmann et al., 2013
The interplay of GbsR and OpcR repressor proteins for opuB and opuC transcription and the compatible solute pools in osmotically stressed cells provides B. subtilis with an effective stress-relieving control unit.
“The interplay of the GbsR and OpcR repressor proteins for opuB and opuC transcription (Nau-Wagner et al., 2012; Lee et al., 2013) and the compatible solute pools in osmotically stressed cells (Hoffmann et al., 2013) provides B. subtilis with an effective stress-relieving control unit.”
From Two MarR-Type Repressors Balance Precursor Uptake and Glycine Betaine Synthesis in Bacillus subtilis to Provide Cytoprotection Against Sustained Osmotic Stress (2020) · cites this paper as Hoffmann et al., 2013
B. subtilis imports compatible solutes such as glycine betaine and proline to rebalance the ionic strength of the cytoplasm.
“To rebalance the ionic strength of the cytoplasm (45), B. subtilis imports compatible solutes such as glycine betaine (GB) and proline (46, 47).”
From A Central Role for Magnesium Homeostasis during Adaptation to Osmotic Stress (2022) · cites this paper as [46]
Increased c-di-AMP inhibits compatible solute uptake by the Opu-family proteins.
“Furthermore, increased c-di-AMP inhibits compatible solute uptake by the Opu-family proteins (35, 46).”
From A Central Role for Magnesium Homeostasis during Adaptation to Osmotic Stress (2022) · cites this paper as [46]
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References 96 · Cited by 109
- Authors
- Hoffmann, T., Wensing, A., Brosius, M., Steil, L., Volker, U., & Bremer, E.
- Affiliations
- Philipps University of Marburg (DE)
- Universität Greifswald (DE)
- Venue
- Journal of Bacteriology
- Publisher
- American Society for Microbiology
- Published
- 2012-11-21
- Volume
- 195
- Issue
- 3
- Pages
- 510-522
- ISSN
- 0021-9193 (ISSN-L)
- PMC
- PMC3554007
- OpenAlex
- W2058359737
- Cited by
- 109
- References
- 96
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 6 · 2023: 7 · 2022: 15 · 2020: 9 · 2019: 5 · 2018: 9 · 2017: 8 · 2016: 5 · 2015: 7 · 2014: 11 · 2013: 9
- FWCI
- 5.20
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Journal of Bacteriology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heat shock proteins research
- Keywords
- OpuA, betaine, proline, osmotic stress, osmoprotection, transcriptional regulation, L-carnitine, choline, Bacillus subtilis, osmolytes
- MeSH terms
- Bacillus subtilis, Bacterial Proteins, Betaine, Escherichia coli, Multigene Family, Osmolar Concentration, Osmotic Pressure, Plasmids, Proline, Sodium Chloride, Gene Expression Regulation, Bacterial, Mutagenesis, Site-Directed, ATP-Binding Cassette Transporters
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