Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth

ABSTRACT Clostridium butyricum, the type species of the genus Clostridium, is considered an obligate anaerobe, yet it has been shown to grow in the presence of oxygen. C. butyricum strains atypically producing the botulinum neurotoxin type E are the leading cause of type E human botulism in Italy. H...

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Autores principales:	Serena Camerini, Lucia Marcocci, Lara Picarazzi, Egidio Iorio, Irene Ruspantini, Paola Pietrangeli, Marco Crescenzi, Giovanna Franciosa
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Clostridium butyricum botulinum neurotoxin oxidative stress Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/24817de69d9148f7a0fb406bfef2ffb4
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spelling	oai:doaj.org-article:24817de69d9148f7a0fb406bfef2ffb42021-12-02T19:46:17ZType E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth10.1128/mSystems.00299-182379-5077https://doaj.org/article/24817de69d9148f7a0fb406bfef2ffb42019-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00299-18https://doaj.org/toc/2379-5077ABSTRACT Clostridium butyricum, the type species of the genus Clostridium, is considered an obligate anaerobe, yet it has been shown to grow in the presence of oxygen. C. butyricum strains atypically producing the botulinum neurotoxin type E are the leading cause of type E human botulism in Italy. Here, we show that type E botulinum neurotoxin-producing C. butyricum strains growing exponentially were able to keep growing and producing toxin in vitro upon exposure to air, although less efficiently than under ideal oxygen-depleted conditions. Bacterial growth in air was maintained when the initial cell density was higher than 103 cells/ml. No spores were detected in the cultures aerated for 5 h. To understand the biological mechanisms allowing the adaptation of vegetative cells of C. butyricum type E to oxygen, we compared the proteome and metabolome profiles of the clostridial cultures grown for 5 h under either aerated or anaerobic conditions. The results indicated that bacterial cells responded to oxygen stress by slowing growth and modulating the expression of proteins involved in carbohydrate uptake and metabolism, redox homeostasis, DNA damage response, and bacterial motility. Moreover, the ratio of acetate to butyrate was significantly higher under aeration. This study demonstrates for the first time that a botulinum neurotoxin-producing Clostridium can withstand oxygen during vegetative growth. IMPORTANCE Botulinum neurotoxins, the causative agents of the potentially fatal disease of botulism, are produced by certain Clostridium strains during vegetative growth, usually in anaerobic environments. Our findings indicate that, contrary to current understanding, the growth of neurotoxigenic C. butyricum strains and botulinum neurotoxin type E production can continue upon transfer from anaerobic to aerated conditions and that adaptation of strains to oxygenated environments requires global changes in proteomic and metabolic profiles. We hypothesize that aerotolerance might constitute an unappreciated factor conferring physiological advantages on some botulinum toxin-producing clostridial strains, allowing them to adapt to otherwise restrictive environments.Serena CameriniLucia MarcocciLara PicarazziEgidio IorioIrene RuspantiniPaola PietrangeliMarco CrescenziGiovanna FranciosaAmerican Society for MicrobiologyarticleClostridium butyricumbotulinum neurotoxinoxidative stressMicrobiologyQR1-502ENmSystems, Vol 4, Iss 2 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Clostridium butyricum botulinum neurotoxin oxidative stress Microbiology QR1-502
spellingShingle	Clostridium butyricum botulinum neurotoxin oxidative stress Microbiology QR1-502 Serena Camerini Lucia Marcocci Lara Picarazzi Egidio Iorio Irene Ruspantini Paola Pietrangeli Marco Crescenzi Giovanna Franciosa Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth
description	ABSTRACT Clostridium butyricum, the type species of the genus Clostridium, is considered an obligate anaerobe, yet it has been shown to grow in the presence of oxygen. C. butyricum strains atypically producing the botulinum neurotoxin type E are the leading cause of type E human botulism in Italy. Here, we show that type E botulinum neurotoxin-producing C. butyricum strains growing exponentially were able to keep growing and producing toxin in vitro upon exposure to air, although less efficiently than under ideal oxygen-depleted conditions. Bacterial growth in air was maintained when the initial cell density was higher than 103 cells/ml. No spores were detected in the cultures aerated for 5 h. To understand the biological mechanisms allowing the adaptation of vegetative cells of C. butyricum type E to oxygen, we compared the proteome and metabolome profiles of the clostridial cultures grown for 5 h under either aerated or anaerobic conditions. The results indicated that bacterial cells responded to oxygen stress by slowing growth and modulating the expression of proteins involved in carbohydrate uptake and metabolism, redox homeostasis, DNA damage response, and bacterial motility. Moreover, the ratio of acetate to butyrate was significantly higher under aeration. This study demonstrates for the first time that a botulinum neurotoxin-producing Clostridium can withstand oxygen during vegetative growth. IMPORTANCE Botulinum neurotoxins, the causative agents of the potentially fatal disease of botulism, are produced by certain Clostridium strains during vegetative growth, usually in anaerobic environments. Our findings indicate that, contrary to current understanding, the growth of neurotoxigenic C. butyricum strains and botulinum neurotoxin type E production can continue upon transfer from anaerobic to aerated conditions and that adaptation of strains to oxygenated environments requires global changes in proteomic and metabolic profiles. We hypothesize that aerotolerance might constitute an unappreciated factor conferring physiological advantages on some botulinum toxin-producing clostridial strains, allowing them to adapt to otherwise restrictive environments.
format	article
author	Serena Camerini Lucia Marcocci Lara Picarazzi Egidio Iorio Irene Ruspantini Paola Pietrangeli Marco Crescenzi Giovanna Franciosa
author_facet	Serena Camerini Lucia Marcocci Lara Picarazzi Egidio Iorio Irene Ruspantini Paola Pietrangeli Marco Crescenzi Giovanna Franciosa
author_sort	Serena Camerini
title	Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth
title_short	Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth
title_full	Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth
title_fullStr	Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth
title_full_unstemmed	Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth
title_sort	type e botulinum neurotoxin-producing <named-content content-type="genus-species">clostridium butyricum</named-content> strains are aerotolerant during vegetative growth
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/24817de69d9148f7a0fb406bfef2ffb4
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Type E Botulinum Neurotoxin-Producing <named-content content-type="genus-species">Clostridium butyricum</named-content> Strains Are Aerotolerant during Vegetative Growth

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