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Food Microbiology

Transcriptional Profile during Deoxycholate-Induced Sporulation in a Clostridium perfringens Isolate Causing Foodborne Illness

Mayo Yasugi, Daisuke Okuzaki, Ritsuko Kuwana, Hiromu Takamatsu, Masaya Fujita, Mahfuzur R. Sarker, Masami Miyake
C. M. Dozois, Editor
Mayo Yasugi
aGraduate School of Life and Environmental Sciences, Osaka Prefecture University, Izumisano, Osaka, Japan
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Daisuke Okuzaki
bDNA Chip Development Center, RIMD, Osaka University, Suita, Osaka, Japan
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Ritsuko Kuwana
cFaculty of Pharmaceutical Sciences, Setsunan University, Hirakata, Osaka, Japan
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Hiromu Takamatsu
cFaculty of Pharmaceutical Sciences, Setsunan University, Hirakata, Osaka, Japan
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Masaya Fujita
dBiology and Biochemistry Department, University of Houston, Houston, Texas, USA
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Mahfuzur R. Sarker
eDepartment of Biomedical Sciences, Oregon State University, Corvallis, Oregon, USA
fDepartment of Microbiology, Oregon State University, Corvallis, Oregon, USA
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Masami Miyake
aGraduate School of Life and Environmental Sciences, Osaka Prefecture University, Izumisano, Osaka, Japan
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C. M. Dozois
INRS–Institut Armand-Frappier
Roles: Editor
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DOI: 10.1128/AEM.00252-16
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ABSTRACT

Clostridium perfringens type A is a common source of foodborne illness (FBI) in humans. Vegetative cells sporulate in the small intestinal tract and produce the major pathogenic factor C. perfringens enterotoxin. Although sporulation plays a critical role in the pathogenesis of FBI, the mechanisms inducing sporulation remain unclear. Bile salts were shown previously to induce sporulation, and we confirmed deoxycholate (DCA)-induced sporulation in C. perfringens strain NCTC8239 cocultured with human intestinal epithelial Caco-2 cells. In the present study, we performed transcriptome analyses of strain NCTC8239 in order to elucidate the mechanism underlying DCA-induced sporulation. Of the 2,761 genes analyzed, 333 were up- or downregulated during DCA-induced sporulation and included genes for cell division, nutrient metabolism, signal transduction, and defense mechanisms. In contrast, the virulence-associated transcriptional regulators (the VirR/VirS system, the agr system, codY, and abrB) were not activated by DCA. DCA markedly increased the expression of signaling molecules controlled by Spo0A, the master regulator of the sporulation process, whereas the expression of spo0A itself was not altered in the presence or absence of DCA. The phosphorylation of Spo0A was enhanced in the presence of DCA. Collectively, these results demonstrated that DCA induced sporulation, at least partially, by facilitating the phosphorylation of Spo0A and activating Spo0A-regulated genes in strain NCTC8239 while altering the expression of various genes.

IMPORTANCE Disease caused by Clostridium perfringens type A consistently ranks among the most common bacterial foodborne illnesses in humans in developed countries. The sporulation of C. perfringens in the small intestinal tract is a key event for its pathogenesis, but the factors and underlying mechanisms by which C. perfringens sporulates in vivo currently remain unclear. Bile salts, major components of bile, which is secreted from the liver for the emulsification of lipids, were shown to induce sporulation. However, the mechanisms underlying bile salt-induced sporulation have not yet been clarified. In the present study, we demonstrate that deoxycholate (one of the bile salts) induces sporulation by facilitating the phosphorylation of Spo0A and activating Spo0A-regulated genes using a transcriptome analysis. Thus, this study enhances our understanding of the mechanisms underlying sporulation, particularly that of bile salt-induced sporulation, in C. perfringens.

FOOTNOTES

    • Received 25 January 2016.
    • Accepted 3 March 2016.
    • Accepted manuscript posted online 11 March 2016.
  • Address correspondence to Mayo Yasugi, shishimaru{at}vet.osakafu-u.ac.jp.
  • Citation Yasugi M, Okuzaki D, Kuwana R, Takamatsu H, Fujita M, Sarker MR, Miyake M. 2016. Transcriptional profile during deoxycholate-induced sporulation in a Clostridium perfringens isolate causing foodborne illness. Appl Environ Microbiol 82:2929–2942. doi:10.1128/AEM.00252-16.

  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/AEM.00252-16.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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Transcriptional Profile during Deoxycholate-Induced Sporulation in a Clostridium perfringens Isolate Causing Foodborne Illness
Mayo Yasugi, Daisuke Okuzaki, Ritsuko Kuwana, Hiromu Takamatsu, Masaya Fujita, Mahfuzur R. Sarker, Masami Miyake
Applied and Environmental Microbiology May 2016, 82 (10) 2929-2942; DOI: 10.1128/AEM.00252-16

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Transcriptional Profile during Deoxycholate-Induced Sporulation in a Clostridium perfringens Isolate Causing Foodborne Illness
Mayo Yasugi, Daisuke Okuzaki, Ritsuko Kuwana, Hiromu Takamatsu, Masaya Fujita, Mahfuzur R. Sarker, Masami Miyake
Applied and Environmental Microbiology May 2016, 82 (10) 2929-2942; DOI: 10.1128/AEM.00252-16
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