The σE regulon and the identification of additional sporulation genes in Bacillus subtilis

Patrick Eichenberger, Shane T. Jensen, Erin M. Conlon, Christiaan Van Ooij, Jessica Silvaggi, José Eduardo González-Pastor, Masaya Fujita, Sigal Ben-Yehuda, Patrick Stragier, Jun S. Liu, Richard Losick

Research output: Contribution to journalArticle

Abstract

We report the identification and characterization on a genome-wide basis of genes under the control of the developmental transcription factor σE in Bacillus subtilis. The σE factor governs gene expression in the larger of the two cellular compartments (the mother cell) created by polar division during the developmental process of sporulation. Using transcriptional profiling and bioinformatics we show that 253 genes (organized in 157 operons) appear to be controlled by σE. Among these, 181 genes (organized in 121 operons) had not been previously described as members of this regulon. Promoters for many of the newly identified genes were located by transcription start site mapping. To assess the role of these genes in sporulation, we created null mutations in 98 of the newly identified genes and operons. Of the resulting mutants, 12 (in prkA, ybaN, yhbH, ykvV, ylbJ, ypjB, yqfC, yqfD, ytrH, ytrI, ytvI and yunB) exhibited defects in spore formation. In addition, subcellular localization studies were carried out using in-frame fusions of several of the genes to the coding sequence for GFP. A majority of the fusion proteins localized either to the membrane surrounding the developing spore or to specific layers of the spore coat, although some fusions showed a uniform distribution in the mother cell cytoplasm. Finally, we used comparative genomics to determine that 46 of the σE-controlled genes in B.subtilis were present in all of the Gram-positive endospore-forming bacteria whose genome has been sequenced, but absent from the genome of the closely related but not endospore-forming bacterium Listeria monocytogenes, thereby defining a core of conserved sporulation genes of probable common ancestral origin. Our findings set the stage for a comprehensive understanding of the contribution of a cell-specific transcription factor to development and morphogenesis.

Original languageEnglish (US)
Pages (from-to)945-972
Number of pages28
JournalJournal of Molecular Biology
Volume327
Issue number5
DOIs
StatePublished - Apr 11 2003

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Regulon
Bacillus subtilis
Genes
Operon
Spores
Genome
Gram-Positive Endospore-Forming Bacteria
Endospore-Forming Bacteria
Transcription Factors
Stem Cells
Transcription Initiation Site
Gene Fusion
Listeria monocytogenes
Genomics
Computational Biology
Morphogenesis
Cytoplasm
Gene Expression
Mutation
Membranes

Keywords

  • Bacillus subtilis
  • Bacterial genomics
  • Protein localization
  • Sigma factors
  • Sporulation

ASJC Scopus subject areas

  • Virology

Cite this

Eichenberger, P., Jensen, S. T., Conlon, E. M., Van Ooij, C., Silvaggi, J., González-Pastor, J. E., ... Losick, R. (2003). The σE regulon and the identification of additional sporulation genes in Bacillus subtilis. Journal of Molecular Biology, 327(5), 945-972. https://doi.org/10.1016/S0022-2836(03)00205-5

The σE regulon and the identification of additional sporulation genes in Bacillus subtilis. / Eichenberger, Patrick; Jensen, Shane T.; Conlon, Erin M.; Van Ooij, Christiaan; Silvaggi, Jessica; González-Pastor, José Eduardo; Fujita, Masaya; Ben-Yehuda, Sigal; Stragier, Patrick; Liu, Jun S.; Losick, Richard.

In: Journal of Molecular Biology, Vol. 327, No. 5, 11.04.2003, p. 945-972.

Research output: Contribution to journalArticle

Eichenberger, P, Jensen, ST, Conlon, EM, Van Ooij, C, Silvaggi, J, González-Pastor, JE, Fujita, M, Ben-Yehuda, S, Stragier, P, Liu, JS & Losick, R 2003, 'The σE regulon and the identification of additional sporulation genes in Bacillus subtilis', Journal of Molecular Biology, vol. 327, no. 5, pp. 945-972. https://doi.org/10.1016/S0022-2836(03)00205-5
Eichenberger, Patrick ; Jensen, Shane T. ; Conlon, Erin M. ; Van Ooij, Christiaan ; Silvaggi, Jessica ; González-Pastor, José Eduardo ; Fujita, Masaya ; Ben-Yehuda, Sigal ; Stragier, Patrick ; Liu, Jun S. ; Losick, Richard. / The σE regulon and the identification of additional sporulation genes in Bacillus subtilis. In: Journal of Molecular Biology. 2003 ; Vol. 327, No. 5. pp. 945-972.
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AU - Van Ooij, Christiaan

AU - Silvaggi, Jessica

AU - González-Pastor, José Eduardo

AU - Fujita, Masaya

AU - Ben-Yehuda, Sigal

AU - Stragier, Patrick

AU - Liu, Jun S.

AU - Losick, Richard

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