Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection

ABSTRACT Bacillus thuringiensis (Bt) is armed to complete a full cycle in its insect host. During infection, virulence factors are expressed under the control of the quorum sensor PlcR to kill the host. After the host's death, the quorum sensor NprR controls a necrotrophic lifestyle, allowing t...

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Autores principales:	Emilie Verplaetse, Leyla Slamti, Michel Gohar, Didier Lereclus
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d9929710bb33412fae3bc049a61824a2
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spelling	oai:doaj.org-article:d9929710bb33412fae3bc049a61824a22021-11-15T15:49:03ZCell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection10.1128/mBio.00138-152150-7511https://doaj.org/article/d9929710bb33412fae3bc049a61824a22015-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00138-15https://doaj.org/toc/2150-7511ABSTRACT Bacillus thuringiensis (Bt) is armed to complete a full cycle in its insect host. During infection, virulence factors are expressed under the control of the quorum sensor PlcR to kill the host. After the host's death, the quorum sensor NprR controls a necrotrophic lifestyle, allowing the vegetative cells to use the insect cadaver as a bioincubator and to survive. Only a part of the Bt population sporulates in the insect cadaver, and the precise composition of the whole population and its evolution over time are unknown. Using fluorescent reporters to record gene expression at the single-cell level, we have determined the differentiation course of a Bt population and explored the lineage existing among virulent, necrotrophic, and sporulating cells. The dynamics of cell differentiation were monitored during growth in homogenized medium, biofilm formation, and colonization of insect larvae. We demonstrated that in the insect host and in planktonic culture in rich medium, the virulence, necrotrophism, and sporulation regulators are successively activated in the same cell. In contrast, in biofilms, activation of PlcR is dispensable for NprR activation and we observed a greater heterogeneity than under the other two growth conditions. We also showed that sporulating cells arise almost exclusively from necrotrophic cells. In biofilm and in the insect cadaver, we identified an as-yet-uncharacterized category of cells that do not express any of the reporters used. Overall, we showed that PlcR, NprR, and Spo0A act as interconnected integrators to allow finely tuned adaptation of the pathogen to its environment. IMPORTANCE Bt is an entomopathogen found ubiquitously in the environment and is a widely used biopesticide. Studies performed at the population level suggest that the infection process of Bt includes three successive steps (virulence, necrotrophism, and sporulation) controlled by different regulators. This study aimed to determine how these phenotypes are activated at the cellular level and if they are switched on in all cells. We used an insect model of infection and biofilms to decipher the cellular differentiation of this bacterium under naturalistic conditions. Our study reveals the connection and lineage existing among virulent, necrotrophic, and sporulating cells. It also shows that the complex conditions encountered in biofilms and during infection generate great heterogeneity inside the population, which might reflect a bet-hedging strategy to ameliorate survival. These data generate new insights into the role of regulatory networks in the adaptation of a pathogen to its host.Emilie VerplaetseLeyla SlamtiMichel GoharDidier LereclusAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 3 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Emilie Verplaetse Leyla Slamti Michel Gohar Didier Lereclus Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection
description	ABSTRACT Bacillus thuringiensis (Bt) is armed to complete a full cycle in its insect host. During infection, virulence factors are expressed under the control of the quorum sensor PlcR to kill the host. After the host's death, the quorum sensor NprR controls a necrotrophic lifestyle, allowing the vegetative cells to use the insect cadaver as a bioincubator and to survive. Only a part of the Bt population sporulates in the insect cadaver, and the precise composition of the whole population and its evolution over time are unknown. Using fluorescent reporters to record gene expression at the single-cell level, we have determined the differentiation course of a Bt population and explored the lineage existing among virulent, necrotrophic, and sporulating cells. The dynamics of cell differentiation were monitored during growth in homogenized medium, biofilm formation, and colonization of insect larvae. We demonstrated that in the insect host and in planktonic culture in rich medium, the virulence, necrotrophism, and sporulation regulators are successively activated in the same cell. In contrast, in biofilms, activation of PlcR is dispensable for NprR activation and we observed a greater heterogeneity than under the other two growth conditions. We also showed that sporulating cells arise almost exclusively from necrotrophic cells. In biofilm and in the insect cadaver, we identified an as-yet-uncharacterized category of cells that do not express any of the reporters used. Overall, we showed that PlcR, NprR, and Spo0A act as interconnected integrators to allow finely tuned adaptation of the pathogen to its environment. IMPORTANCE Bt is an entomopathogen found ubiquitously in the environment and is a widely used biopesticide. Studies performed at the population level suggest that the infection process of Bt includes three successive steps (virulence, necrotrophism, and sporulation) controlled by different regulators. This study aimed to determine how these phenotypes are activated at the cellular level and if they are switched on in all cells. We used an insect model of infection and biofilms to decipher the cellular differentiation of this bacterium under naturalistic conditions. Our study reveals the connection and lineage existing among virulent, necrotrophic, and sporulating cells. It also shows that the complex conditions encountered in biofilms and during infection generate great heterogeneity inside the population, which might reflect a bet-hedging strategy to ameliorate survival. These data generate new insights into the role of regulatory networks in the adaptation of a pathogen to its host.
format	article
author	Emilie Verplaetse Leyla Slamti Michel Gohar Didier Lereclus
author_facet	Emilie Verplaetse Leyla Slamti Michel Gohar Didier Lereclus
author_sort	Emilie Verplaetse
title	Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection
title_short	Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection
title_full	Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection
title_fullStr	Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection
title_full_unstemmed	Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection
title_sort	cell differentiation in a <named-content content-type="genus-species">bacillus thuringiensis</named-content> population during planktonic growth, biofilm formation, and host infection
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/d9929710bb33412fae3bc049a61824a2
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Cell Differentiation in a <named-content content-type="genus-species">Bacillus thuringiensis</named-content> Population during Planktonic Growth, Biofilm Formation, and Host Infection

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