Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations

ABSTRACT Vibrio cholerae represents both an environmental pathogen and a widely distributed microbial species comprised of closely related strains occurring in the tropical to temperate coastal ocean across the globe (Colwell RR, Science 274:2025–2031, 1996; Griffith DC, Kelly-Hope LA, Miller MA, Am...

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Autores principales:	Yan Boucher, Otto X. Cordero, Alison Takemura, Dana E. Hunt, Klaus Schliep, Eric Bapteste, Philippe Lopez, Cheryl L. Tarr, Martin F. Polz
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/b69924955c234de28fe0e69b0b3cff0a
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spelling	oai:doaj.org-article:b69924955c234de28fe0e69b0b3cff0a2021-11-15T15:39:08ZLocal Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations10.1128/mBio.00335-102150-7511https://doaj.org/article/b69924955c234de28fe0e69b0b3cff0a2011-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00335-10https://doaj.org/toc/2150-7511ABSTRACT Vibrio cholerae represents both an environmental pathogen and a widely distributed microbial species comprised of closely related strains occurring in the tropical to temperate coastal ocean across the globe (Colwell RR, Science 274:2025–2031, 1996; Griffith DC, Kelly-Hope LA, Miller MA, Am. J. Trop. Med. Hyg. 75:973–977, 2006; Reidl J, Klose KE, FEMS Microbiol. Rev. 26:125–139, 2002). However, although this implies dispersal and growth across diverse environmental conditions, how locally successful populations assemble from a possibly global gene pool, relatively unhindered by geographic boundaries, remains poorly understood. Here, we show that environmental Vibrio cholerae possesses two, largely distinct gene pools: one is vertically inherited and globally well mixed, and the other is local and rapidly transferred across species boundaries to generate an endemic population structure. While phylogeographic analysis of isolates collected from Bangladesh and the U.S. east coast suggested strong panmixis for protein-coding genes, there was geographic structure in integrons, which are the only genomic islands present in all strains of V. cholerae (Chun J, et al., Proc. Natl. Acad. Sci. U. S. A. 106:15442–15447, 2009) and are capable of acquiring and expressing mobile gene cassettes. Geographic differentiation in integrons arises from high gene turnover, with acquisition from a locally cooccurring sister species being up to twice as likely as exchange with conspecific but geographically distant V. cholerae populations. IMPORTANCE Functional predictions of integron genes show the predominance of secondary metabolism and cell surface modification, which is consistent with a role in competition and predation defense. We suggest that the integron gene pool’s distinctness and tempo of sharing are adaptive in allowing rapid conversion of genomes to reflect local ecological constraints. Because the integron is frequently the main element differentiating clinical strains (Chun J, et al., Proc. Natl. Acad. Sci. U. S. A. 106:15442–15447, 2009) and its recombinogenic activity is directly stimulated by environmental stresses (Guerin E, et al., Science 324:1034, 2009), these observations are relevant for local emergence and subsequent dispersal.Yan BoucherOtto X. CorderoAlison TakemuraDana E. HuntKlaus SchliepEric BaptestePhilippe LopezCheryl L. TarrMartin F. PolzAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 2 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Yan Boucher Otto X. Cordero Alison Takemura Dana E. Hunt Klaus Schliep Eric Bapteste Philippe Lopez Cheryl L. Tarr Martin F. Polz Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations
description	ABSTRACT Vibrio cholerae represents both an environmental pathogen and a widely distributed microbial species comprised of closely related strains occurring in the tropical to temperate coastal ocean across the globe (Colwell RR, Science 274:2025–2031, 1996; Griffith DC, Kelly-Hope LA, Miller MA, Am. J. Trop. Med. Hyg. 75:973–977, 2006; Reidl J, Klose KE, FEMS Microbiol. Rev. 26:125–139, 2002). However, although this implies dispersal and growth across diverse environmental conditions, how locally successful populations assemble from a possibly global gene pool, relatively unhindered by geographic boundaries, remains poorly understood. Here, we show that environmental Vibrio cholerae possesses two, largely distinct gene pools: one is vertically inherited and globally well mixed, and the other is local and rapidly transferred across species boundaries to generate an endemic population structure. While phylogeographic analysis of isolates collected from Bangladesh and the U.S. east coast suggested strong panmixis for protein-coding genes, there was geographic structure in integrons, which are the only genomic islands present in all strains of V. cholerae (Chun J, et al., Proc. Natl. Acad. Sci. U. S. A. 106:15442–15447, 2009) and are capable of acquiring and expressing mobile gene cassettes. Geographic differentiation in integrons arises from high gene turnover, with acquisition from a locally cooccurring sister species being up to twice as likely as exchange with conspecific but geographically distant V. cholerae populations. IMPORTANCE Functional predictions of integron genes show the predominance of secondary metabolism and cell surface modification, which is consistent with a role in competition and predation defense. We suggest that the integron gene pool’s distinctness and tempo of sharing are adaptive in allowing rapid conversion of genomes to reflect local ecological constraints. Because the integron is frequently the main element differentiating clinical strains (Chun J, et al., Proc. Natl. Acad. Sci. U. S. A. 106:15442–15447, 2009) and its recombinogenic activity is directly stimulated by environmental stresses (Guerin E, et al., Science 324:1034, 2009), these observations are relevant for local emergence and subsequent dispersal.
format	article
author	Yan Boucher Otto X. Cordero Alison Takemura Dana E. Hunt Klaus Schliep Eric Bapteste Philippe Lopez Cheryl L. Tarr Martin F. Polz
author_facet	Yan Boucher Otto X. Cordero Alison Takemura Dana E. Hunt Klaus Schliep Eric Bapteste Philippe Lopez Cheryl L. Tarr Martin F. Polz
author_sort	Yan Boucher
title	Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations
title_short	Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations
title_full	Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations
title_fullStr	Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations
title_full_unstemmed	Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations
title_sort	local mobile gene pools rapidly cross species boundaries to create endemicity within global <named-content content-type="genus-species">vibrio cholerae</named-content> populations
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/b69924955c234de28fe0e69b0b3cff0a
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Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global <named-content content-type="genus-species">Vibrio cholerae</named-content> Populations

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