Dual-Specificity Anti-sigma Factor Reinforces Control of Cell-Type Specific Gene Expression in Bacillus subtilis

Mónica Serrano, JinXin X. Gao, João Bota, Ashley R. Bate, Jeffrey Meisner, Patrick Eichenberger, Charles P. Moran, Adriano O. Henriques

Research output: Contribution to journalArticle

Abstract

Gene expression during spore development in Bacillus subtilis is controlled by cell type-specific RNA polymerase sigma factors. σ<sup>F</sup>and σ<sup>E</sup> control early stages of development in the forespore and the mother cell, respectively. When, at an intermediate stage in development, the mother cell engulfs the forespore, σ<sup>F</sup> is replaced by σ<sup>G</sup> and σ<sup>E</sup> is replaced by σ<sup>K</sup>. The anti-sigma factor CsfB is produced under the control of σ<sup>F</sup> and binds to and inhibits the auto-regulatory σ<sup>G</sup>, but not σ<sup>F</sup>. A position in region 2.1, occupied by an asparagine in σ<sup>G</sup> and by a glutamate in ο<sup>F</sup>, is sufficient for CsfB discrimination of the two sigmas, and allows it to delay the early to late switch in forespore gene expression. We now show that following engulfment completion, csfB is switched on in the mother cell under the control of σ<sup>K</sup> and that CsfB binds to and inhibits σ<sup>E</sup> but not σ<sup>K</sup>, possibly to facilitate the switch from early to late gene expression. We show that a position in region 2.3 occupied by a conserved asparagine in σ<sup>E</sup> and by a conserved glutamate in σ<sup>K</sup> suffices for discrimination by CsfB. We also show that CsfB prevents activation of σ<sup>G</sup> in the mother cell and the premature σ<sup>G</sup>-dependent activation of σ<sup>K</sup>. Thus, CsfB establishes negative feedback loops that curtail the activity of σ<sup>E</sup> and prevent the ectopic activation of σ<sup>G</sup> in the mother cell. The capacity of CsfB to directly block σ<sup>E</sup> activity may also explain how CsfB plays a role as one of the several mechanisms that prevent σ<sup>E</sup> activation in the forespore. Thus the capacity of CsfB to differentiate between the highly similar σ<sup>F</sup>/σ<sup>G</sup> and σ<sup>E</sup>/σ<sup>K</sup> pairs allows it to rinforce the cell-type specificity of these sigma factors and the transition from early to late development in B. subtilis, and possibly in all sporeformers that encode a CsfB orthologue.

Original languageEnglish (US)
Article numbere1005104
JournalPLoS Genetics
Volume11
Issue number3
DOIs
StatePublished - Apr 2 2015

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sigma factors
Sigma Factor
Bacillus subtilis
gene expression
Stem Cells
Gene Expression
Asparagine
cells
Glutamic Acid
asparagine
RNA
spore
glutamates
DNA-Directed RNA Polymerases
Spores
DNA-directed RNA polymerase
automobiles
spores

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Cancer Research
  • Genetics(clinical)

Cite this

Dual-Specificity Anti-sigma Factor Reinforces Control of Cell-Type Specific Gene Expression in Bacillus subtilis. / Serrano, Mónica; Gao, JinXin X.; Bota, João; Bate, Ashley R.; Meisner, Jeffrey; Eichenberger, Patrick; Moran, Charles P.; Henriques, Adriano O.

In: PLoS Genetics, Vol. 11, No. 3, e1005104, 02.04.2015.

Research output: Contribution to journalArticle

Serrano, Mónica ; Gao, JinXin X. ; Bota, João ; Bate, Ashley R. ; Meisner, Jeffrey ; Eichenberger, Patrick ; Moran, Charles P. ; Henriques, Adriano O. / Dual-Specificity Anti-sigma Factor Reinforces Control of Cell-Type Specific Gene Expression in Bacillus subtilis. In: PLoS Genetics. 2015 ; Vol. 11, No. 3.
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AU - Bota, João

AU - Bate, Ashley R.

AU - Meisner, Jeffrey

AU - Eichenberger, Patrick

AU - Moran, Charles P.

AU - Henriques, Adriano O.

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