Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System

ABSTRACT Clostridium perfringens type B and D strains cause enterotoxemias and enteritis in livestock after proliferating in the intestines and producing epsilon-toxin (ETX), alpha-toxin (CPA), and, usually, perfringolysin O (PFO). Although ETX is one of the most potent bacterial toxins, the regulat...

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Autores principales:	Jianming Chen, Julian I. Rood, Bruce A. McClane
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b1881a118a2344a4b8b515cd013d26fc
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spelling	oai:doaj.org-article:b1881a118a2344a4b8b515cd013d26fc2021-11-15T15:38:48ZEpsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System10.1128/mBio.00275-112150-7511https://doaj.org/article/b1881a118a2344a4b8b515cd013d26fc2011-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00275-11https://doaj.org/toc/2150-7511ABSTRACT Clostridium perfringens type B and D strains cause enterotoxemias and enteritis in livestock after proliferating in the intestines and producing epsilon-toxin (ETX), alpha-toxin (CPA), and, usually, perfringolysin O (PFO). Although ETX is one of the most potent bacterial toxins, the regulation of ETX production by type B or D strains remains poorly understood. The present work determined that the type D strain CN3718 upregulates production of ETX upon close contact with enterocyte-like Caco-2 cells. This host cell-induced upregulation of ETX expression was mediated at the transcriptional level. Using an isogenic agrB null mutant and complemented strain, the agr operon was shown to be required when CN3718 produces ETX in broth culture or, via a secreted signal consistent with a quorum-sensing (QS) effect, upregulates ETX production upon contact with host cells. These findings provide the first insights into the regulation of ETX production, as well as additional evidence that the Agr-like QS system functions as a global regulator of C. perfringens toxin production. Since it was proposed previously that the Agr-like QS system regulates C. perfringens gene expression via the VirS/VirR two-component regulatory system, an isogenic virR null mutant of CN3718 was constructed to evaluate the importance of VirS/VirR for CN3718 toxin production. This mutation affected production of CPA and PFO, but not ETX, by CN3718. These results provide the first indication that C. perfringens toxin expression regulation by the Agr-like quorum-sensing system may not always act via the VirS/VirR two-component system. IMPORTANCE Mechanisms by which Clostridium perfringens type B and D strains regulate production of epsilon-toxin (ETX), a CDC class B select toxin, are poorly understood. Production of several other toxins expressed by C. perfringens is wholly or partially regulated by both the Agr-like quorum-sensing (QS) system and the VirS/VirR two-component regulatory system, so the present study tested whether ETX expression by type D strain CN3718 also requires these regulatory systems. The agr operon was shown to be essential for signaling CN3718 to produce ETX in broth culture or to upregulate ETX production upon close contact with enterocyte-like Caco-2 cells, which may have pathogenic relevance since ETX is produced intestinally. However, ETX production remained at wild-type levels after inactivation of the VirS/VirR system in CN3718. These findings provide the first information regarding regulation of ETX production and suggest Agr-like QS toxin production regulation in C. perfringens does not always require the VirS/VirR system.Jianming ChenJulian I. RoodBruce A. McClaneAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 6 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Jianming Chen Julian I. Rood Bruce A. McClane Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System
description	ABSTRACT Clostridium perfringens type B and D strains cause enterotoxemias and enteritis in livestock after proliferating in the intestines and producing epsilon-toxin (ETX), alpha-toxin (CPA), and, usually, perfringolysin O (PFO). Although ETX is one of the most potent bacterial toxins, the regulation of ETX production by type B or D strains remains poorly understood. The present work determined that the type D strain CN3718 upregulates production of ETX upon close contact with enterocyte-like Caco-2 cells. This host cell-induced upregulation of ETX expression was mediated at the transcriptional level. Using an isogenic agrB null mutant and complemented strain, the agr operon was shown to be required when CN3718 produces ETX in broth culture or, via a secreted signal consistent with a quorum-sensing (QS) effect, upregulates ETX production upon contact with host cells. These findings provide the first insights into the regulation of ETX production, as well as additional evidence that the Agr-like QS system functions as a global regulator of C. perfringens toxin production. Since it was proposed previously that the Agr-like QS system regulates C. perfringens gene expression via the VirS/VirR two-component regulatory system, an isogenic virR null mutant of CN3718 was constructed to evaluate the importance of VirS/VirR for CN3718 toxin production. This mutation affected production of CPA and PFO, but not ETX, by CN3718. These results provide the first indication that C. perfringens toxin expression regulation by the Agr-like quorum-sensing system may not always act via the VirS/VirR two-component system. IMPORTANCE Mechanisms by which Clostridium perfringens type B and D strains regulate production of epsilon-toxin (ETX), a CDC class B select toxin, are poorly understood. Production of several other toxins expressed by C. perfringens is wholly or partially regulated by both the Agr-like quorum-sensing (QS) system and the VirS/VirR two-component regulatory system, so the present study tested whether ETX expression by type D strain CN3718 also requires these regulatory systems. The agr operon was shown to be essential for signaling CN3718 to produce ETX in broth culture or to upregulate ETX production upon close contact with enterocyte-like Caco-2 cells, which may have pathogenic relevance since ETX is produced intestinally. However, ETX production remained at wild-type levels after inactivation of the VirS/VirR system in CN3718. These findings provide the first information regarding regulation of ETX production and suggest Agr-like QS toxin production regulation in C. perfringens does not always require the VirS/VirR system.
format	article
author	Jianming Chen Julian I. Rood Bruce A. McClane
author_facet	Jianming Chen Julian I. Rood Bruce A. McClane
author_sort	Jianming Chen
title	Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System
title_short	Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System
title_full	Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System
title_fullStr	Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System
title_full_unstemmed	Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System
title_sort	epsilon-toxin production by <named-content content-type="genus-species">clostridium perfringens</named-content> type d strain cn3718 is dependent upon the <italic toggle="yes">agr</italic> operon but not the virs/virr two-component regulatory system
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/b1881a118a2344a4b8b515cd013d26fc
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Epsilon-Toxin Production by <named-content content-type="genus-species">Clostridium perfringens</named-content> Type D Strain CN3718 Is Dependent upon the <italic toggle="yes">agr</italic> Operon but Not the VirS/VirR Two-Component Regulatory System

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