Academic Journal
The Master Regulator Spo0A Integrates DNA Sequence and Shape to Regulate the Sporulation Kinase Gene kinA in Bacillus subtilis.
| Τίτλος: | The Master Regulator Spo0A Integrates DNA Sequence and Shape to Regulate the Sporulation Kinase Gene kinA in Bacillus subtilis. |
|---|---|
| Συγγραφείς: | Zahid SH; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA., Zarazúa-Osorio B; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA., Escobedo R; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA., Ullah S; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA., Dona SKK; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA., Fujita M; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA. |
| Πηγή: | Molecular microbiology [Mol Microbiol] 2026 Oct; Vol. 126 (4), pp. 359-378. Date of Electronic Publication: 2026 Jul 28. |
| Τύπος έκδοσης: | Journal Article |
| Γλώσσα: | English |
| Στοιχεία περιοδικού: | Publisher: Blackwell Scientific Publications Country of Publication: England NLM ID: 8712028 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-2958 (Electronic) Linking ISSN: 0950382X NLM ISO Abbreviation: Mol Microbiol Subsets: MEDLINE |
| Imprint Name(s): | Original Publication: Oxford, OX ; Boston, MA : Blackwell Scientific Publications, c1987- |
| Ιατρικοί όροι (MeSH): | Bacillus subtilis*/genetics , Bacillus subtilis*/metabolism , Bacterial Proteins*/genetics , Bacterial Proteins*/metabolism , Protein Kinases*/genetics , Protein Kinases*/metabolism , Transcription Factors*/metabolism , Transcription Factors*/genetics, Gene Expression Regulation, Bacterial/genetics ; Spores, Bacterial/genetics ; Spores, Bacterial/metabolism ; DNA, Bacterial/genetics ; DNA, Bacterial/metabolism ; Promoter Regions, Genetic ; Phosphorylation ; Transcription, Genetic |
| Περίληψη: | Sporulation in starved Bacillus subtilis depends on precise control of kinA, which encodes the major phosphorelay kinase that generates the threshold level of phosphorylated Spo0A (Spo0A~P) required for entry into sporulation. Here, we define the regulatory logic that shapes kinA expression and uncover structural features that influence Spo0A~P recruitment. First, we show that the kinA promoter integrates positive and negative Spo0A~P inputs through a composite three-site 0A-box architecture. Distinct affinities and cooperative interactions among the three sites generate a controlled output in which activating and repressive inputs are balanced during starvation, maintaining basal-to-moderate kinA transcription. Second, we identify intrinsic DNA bending as a sequence-independent mechanism that enhances Spo0A~P engagement, promoting low-specificity interactions that may contribute to transcriptional regulation and more broadly chromosome organization. Finally, we show that both the kinA promoter and KinA protein domains diverge between pathogenic and nonpathogenic Bacillus species, reflecting niche-specific evolutionary pressures on sporulation initiation. Together, these findings support an integrated model in which promoter architecture and DNA shape collectively tune Spo0A~P dependent regulation of kinA. (© 2026 John Wiley & Sons Ltd.) |
| References: | Ben‐Yehuda, S., D. Z. Rudner, and R. Losick. 2003. “RacA, a Bacterial Protein That Anchors Chromosomes to the Cell Poles.” Science 299: 532–536. Bossi, L., and D. M. Smith. 1984. “Conformational Change in the DNA Associated With an Unusual Promoter Mutation in a tRNA Operon of Salmonella.” Cell 39: 643–652. Burbulys, D., K. A. Trach, and J. A. Hoch. 1991. “Initiation of Sporulation in B. subtilis Is Controlled by a Multicomponent Phosphorelay.” Cell 64: 545–552. Carniol, K., P. Eichenberger, and R. Losick. 2004. “A Threshold Mechanism Governing Activation of the Developmental Regulatory Protein Sigma F in Bacillus subtilis.” Journal of Biological Chemistry 279: 14860–14870. Chastanet, A., and R. Losick. 2011. “Just‐In‐Time Control of Spo0A Synthesis in Bacillus subtilis by Multiple Regulatory Mechanisms.” Journal of Bacteriology 193: 6366–6374. Chen, Z., P. Srivastava, B. Zarazua‐Osorio, A. Marathe, M. Fujita, and O. A. 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| Grant Information: | E-2099-20220331 Welch Foundation |
| Contributed Indexing: | Keywords: Bacillus subtilis; histidine kinase; phosphorelay; response regulator; sporulation Local Abstract: [plain-language-summary] Spore‐forming bacteria survive starvation by entering sporulation, but how this developmental switch is controlled is not fully understood. We show that the master regulator Spo0A controls the major sporulation kinase gene kinA through three DNA‐binding sites and the shape of the DNA itself. Together, these features help regulate the transition from growth to sporulation. |
| Substance Nomenclature: | 0 (Bacterial Proteins) 0 (Spo0A protein, Bacillus subtilis) EC 2.7.- (Protein Kinases) 0 (Transcription Factors) 0 (kinA protein, Bacillus subtilis) 0 (DNA, Bacterial) |
| Entry Date(s): | Date Created: 20260728 Date Completed: 20261007 Latest Revision: 20261007 |
| Update Code: | 20261008 |
| DOI: | 10.1111/mmi.70100 |
| PMID: | 42520298 |
| Βάση Δεδομένων: | MEDLINE |
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| Items | – Name: Title Label: Title Group: Ti Data: The Master Regulator Spo0A Integrates DNA Sequence and Shape to Regulate the Sporulation Kinase Gene kinA in Bacillus subtilis. – Name: Author Label: Authors Group: Au Data: <searchLink fieldCode="AU" term="%22Zahid+SH%22">Zahid SH</searchLink>; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA.<br /><searchLink fieldCode="AU" term="%22Zarazúa-Osorio+B%22">Zarazúa-Osorio B</searchLink>; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA.<br /><searchLink fieldCode="AU" term="%22Escobedo+R%22">Escobedo R</searchLink>; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA.<br /><searchLink fieldCode="AU" term="%22Ullah+S%22">Ullah S</searchLink>; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA.<br /><searchLink fieldCode="AU" term="%22Dona+SKK%22">Dona SKK</searchLink>; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA.<br /><searchLink fieldCode="AU" term="%22Fujita+M%22">Fujita M</searchLink>; Department of Biology and Biochemistry, University of Houston, Houston, Texas, USA. – Name: TitleSource Label: Source Group: Src Data: <searchLink fieldCode="JN" term="%228712028%22">Molecular microbiology</searchLink> [Mol Microbiol] 2026 Oct; Vol. 126 (4), pp. 359-378. <i>Date of Electronic Publication: </i>2026 Jul 28. – Name: TypePub Label: Publication Type Group: TypPub Data: Journal Article – Name: Language Label: Language Group: Lang Data: English – Name: TitleSource Label: Journal Info Group: Src Data: <i>Publisher: </i><searchLink fieldCode="PB" term="%22Blackwell+Scientific+Publications%22">Blackwell Scientific Publications </searchLink><i>Country of Publication: </i>England <i>NLM ID: </i>8712028 <i>Publication Model: </i>Print-Electronic <i>Cited Medium: </i>Internet <i>ISSN: </i>1365-2958 (Electronic) <i>Linking ISSN: </i><searchLink fieldCode="IS" term="%220950382X%22">0950382X </searchLink><i>NLM ISO Abbreviation: </i>Mol Microbiol <i>Subsets: </i>MEDLINE – Name: PublisherInfo Label: Imprint Name(s) Group: PubInfo Data: <i>Original Publication</i>: Oxford, OX ; Boston, MA : Blackwell Scientific Publications, c1987- – Name: SubjectMESH Label: MeSH Terms Group: Su Data: <searchLink fieldCode="MM" term="%22Bacillus+subtilis%22">Bacillus subtilis*</searchLink>/<searchLink fieldCode="MM" term="%22Bacillus+subtilis+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacillus+subtilis%22">Bacillus subtilis*</searchLink>/<searchLink fieldCode="MM" term="%22Bacillus+subtilis+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacterial+Proteins%22">Bacterial Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Bacterial+Proteins+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Bacterial+Proteins%22">Bacterial Proteins*</searchLink>/<searchLink fieldCode="MM" term="%22Bacterial+Proteins+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Protein+Kinases%22">Protein Kinases*</searchLink>/<searchLink fieldCode="MM" term="%22Protein+Kinases+genetics%22">genetics</searchLink> <br /><searchLink fieldCode="MM" term="%22Protein+Kinases%22">Protein Kinases*</searchLink>/<searchLink fieldCode="MM" term="%22Protein+Kinases+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Transcription+Factors%22">Transcription Factors*</searchLink>/<searchLink fieldCode="MM" term="%22Transcription+Factors+metabolism%22">metabolism</searchLink> <br /><searchLink fieldCode="MM" term="%22Transcription+Factors%22">Transcription Factors*</searchLink>/<searchLink fieldCode="MM" term="%22Transcription+Factors+genetics%22">genetics</searchLink><br /><searchLink fieldCode="MH" term="%22Gene+Expression+Regulation%2C+Bacterial%22">Gene Expression Regulation, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22Gene+Expression+Regulation%2C+Bacterial+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Spores%2C+Bacterial%22">Spores, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22Spores%2C+Bacterial+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22Spores%2C+Bacterial%22">Spores, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22Spores%2C+Bacterial+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22DNA%2C+Bacterial%22">DNA, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22DNA%2C+Bacterial+genetics%22">genetics</searchLink> ; <searchLink fieldCode="MH" term="%22DNA%2C+Bacterial%22">DNA, Bacterial</searchLink>/<searchLink fieldCode="MH" term="%22DNA%2C+Bacterial+metabolism%22">metabolism</searchLink> ; <searchLink fieldCode="MH" term="%22Promoter+Regions%2C+Genetic%22">Promoter Regions, Genetic</searchLink> ; <searchLink fieldCode="MH" term="%22Phosphorylation%22">Phosphorylation</searchLink> ; <searchLink fieldCode="MH" term="%22Transcription%2C+Genetic%22">Transcription, Genetic</searchLink> – Name: Abstract Label: Abstract Group: Ab Data: Sporulation in starved Bacillus subtilis depends on precise control of kinA, which encodes the major phosphorelay kinase that generates the threshold level of phosphorylated Spo0A (Spo0A~P) required for entry into sporulation. Here, we define the regulatory logic that shapes kinA expression and uncover structural features that influence Spo0A~P recruitment. First, we show that the kinA promoter integrates positive and negative Spo0A~P inputs through a composite three-site 0A-box architecture. Distinct affinities and cooperative interactions among the three sites generate a controlled output in which activating and repressive inputs are balanced during starvation, maintaining basal-to-moderate kinA transcription. Second, we identify intrinsic DNA bending as a sequence-independent mechanism that enhances Spo0A~P engagement, promoting low-specificity interactions that may contribute to transcriptional regulation and more broadly chromosome organization. Finally, we show that both the kinA promoter and KinA protein domains diverge between pathogenic and nonpathogenic Bacillus species, reflecting niche-specific evolutionary pressures on sporulation initiation. Together, these findings support an integrated model in which promoter architecture and DNA shape collectively tune Spo0A~P dependent regulation of kinA.<br /> (© 2026 John Wiley & Sons Ltd.) – Name: Ref Label: References Group: RefInfo Data: Ben‐Yehuda, S., D. Z. Rudner, and R. Losick. 2003. “RacA, a Bacterial Protein That Anchors Chromosomes to the Cell Poles.” Science 299: 532–536.<br />Bossi, L., and D. M. Smith. 1984. “Conformational Change in the DNA Associated With an Unusual Promoter Mutation in a tRNA Operon of Salmonella.” Cell 39: 643–652.<br />Burbulys, D., K. A. Trach, and J. A. Hoch. 1991. “Initiation of Sporulation in B. subtilis Is Controlled by a Multicomponent Phosphorelay.” Cell 64: 545–552.<br />Carniol, K., P. Eichenberger, and R. Losick. 2004. “A Threshold Mechanism Governing Activation of the Developmental Regulatory Protein Sigma F in Bacillus subtilis.” Journal of Biological Chemistry 279: 14860–14870.<br />Chastanet, A., and R. 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Wu. 2018. “The Complete Genome Sequence of Bacillus Halotolerans ZB201702 Isolated From a Drought‐ and Salt‐Stressed Rhizosphere Soil.” Microbial Pathogenesis 123: 246–249. – Name: GrantInfo Label: Grant Information Group: Grant Data: E-2099-20220331 Welch Foundation – Name: SubjectMinor Label: Contributed Indexing Group: Data: <i>Keywords: </i>Bacillus subtilis; histidine kinase; phosphorelay; response regulator; sporulation<br /><i>Local Abstract: </i>[plain-language-summary] Spore‐forming bacteria survive starvation by entering sporulation, but how this developmental switch is controlled is not fully understood. We show that the master regulator Spo0A controls the major sporulation kinase gene kinA through three DNA‐binding sites and the shape of the DNA itself. Together, these features help regulate the transition from growth to sporulation. – Name: NumberCAS Label: Substance Nomenclature Group: ID Data: 0 (Bacterial Proteins)<br />0 (Spo0A protein, Bacillus subtilis)<br />EC 2.7.- (Protein Kinases)<br />0 (Transcription Factors)<br />0 (kinA protein, Bacillus subtilis)<br />0 (DNA, Bacterial) – Name: DateEntry Label: Entry Date(s) Group: Date Data: <i>Date Created: </i>20260728 <i>Date Completed: </i>20261007 <i>Latest Revision: </i>20261007 – Name: DateUpdate Label: Update Code Group: Date Data: 20261008 – Name: DOI Label: DOI Group: ID Data: 10.1111/mmi.70100 – Name: AN Label: PMID Group: ID Data: 42520298 |
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| RecordInfo | BibRecord: BibEntity: Identifiers: – Type: doi Value: 10.1111/mmi.70100 Languages: – Code: eng Text: English PhysicalDescription: Pagination: StartPage: 359 Subjects: – SubjectFull: Gene Expression Regulation, Bacterial genetics Type: general – SubjectFull: Spores, Bacterial genetics Type: general – SubjectFull: Spores, Bacterial metabolism Type: general – SubjectFull: DNA, Bacterial genetics Type: general – SubjectFull: DNA, Bacterial metabolism Type: general – SubjectFull: Promoter Regions, Genetic Type: general – SubjectFull: Phosphorylation Type: general – SubjectFull: Transcription, Genetic Type: general – SubjectFull: Bacillus subtilis genetics Type: general – SubjectFull: Bacillus subtilis metabolism Type: general – SubjectFull: Bacterial Proteins genetics Type: general – SubjectFull: Bacterial Proteins metabolism Type: general – SubjectFull: Protein Kinases genetics Type: general – SubjectFull: Protein Kinases metabolism Type: general – SubjectFull: Transcription Factors metabolism Type: general – SubjectFull: Transcription Factors genetics Type: general Titles: – TitleFull: The Master Regulator Spo0A Integrates DNA Sequence and Shape to Regulate the Sporulation Kinase Gene kinA in Bacillus subtilis. Type: main BibRelationships: HasContributorRelationships: – PersonEntity: Name: NameFull: Zahid SH – PersonEntity: Name: NameFull: Zarazúa-Osorio B – PersonEntity: Name: NameFull: Escobedo R – PersonEntity: Name: NameFull: Ullah S – PersonEntity: Name: NameFull: Dona SKK – PersonEntity: Name: NameFull: Fujita M IsPartOfRelationships: – BibEntity: Dates: – D: 01 M: 10 Text: 2026 Oct Type: published Y: 2026 Identifiers: – Type: issn-electronic Value: 1365-2958 Numbering: – Type: volume Value: 126 – Type: issue Value: 4 Titles: – TitleFull: Molecular microbiology Type: main |
| ResultId | 1 |