Giuseppe
Emeritus
Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global Vibrio cholerae Populations (mBio, abstract, edited)
[Source: mBio, full text: <cite cite="http://mbio.asm.org/content/2/2/e00335-10.short?rss=1">Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global Vibrio cholerae Populations</cite>. Abstract, edited.]
Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global Vibrio cholerae Populations
1. Yan Boucher a*, 2. Otto X. Cordero a, 3. Alison Takemura a, 4. Dana E. Hunt b, 5. Klaus Schliep c, 6. Eric Bapteste c, 7. Philippe Lopez c, 8. Cheryl L. Tarr d, and 9. Martin F. Polz a
Author Affiliations
1. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA (a);
2. Nicholas School of the Environment, Duke University, Durham, North Carolina, USA (b);
3. Unit? Mixte de Recherche, Centre National de Recherche Scientifique 7138, Syst?matique, Adaptation, Evolution, Universit? Pierre et Marie Curie, 75005 Paris, France (c); and
4. Listeria, Yersinia, Vibrio and Enterobacteriaceae Reference Laboratories, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA (d)
Author Notes
* ↵* Present address: Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada.
1. Address correspondence to Yan Boucher, yboucher@ualberta.ca, or Martin F. Polz, mpolz@mit.edu.
1. Editor David Relman, VA Palo Alto Health Care System
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.
Footnotes
* Citation Boucher Y, et al. 2011. Local mobile gene pools rapidly cross species boundaries to create endemicity within global Vibrio cholerae populations. mBio 2(2):e00335-10. doi:10.1128/mBio.00335-10.
* Received 18 December 2010
* Accepted 22 March 2011
* Published 12 April 2011
* Copyright ? 2011 Boucher et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
-
-----
[Source: mBio, full text: <cite cite="http://mbio.asm.org/content/2/2/e00335-10.short?rss=1">Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global Vibrio cholerae Populations</cite>. Abstract, edited.]
Local Mobile Gene Pools Rapidly Cross Species Boundaries To Create Endemicity within Global Vibrio cholerae Populations
1. Yan Boucher a*, 2. Otto X. Cordero a, 3. Alison Takemura a, 4. Dana E. Hunt b, 5. Klaus Schliep c, 6. Eric Bapteste c, 7. Philippe Lopez c, 8. Cheryl L. Tarr d, and 9. Martin F. Polz a
Author Affiliations
1. Department of Civil and Environmental Engineering, Massachusetts Institute of Technology (MIT), Cambridge, Massachusetts, USA (a);
2. Nicholas School of the Environment, Duke University, Durham, North Carolina, USA (b);
3. Unit? Mixte de Recherche, Centre National de Recherche Scientifique 7138, Syst?matique, Adaptation, Evolution, Universit? Pierre et Marie Curie, 75005 Paris, France (c); and
4. Listeria, Yersinia, Vibrio and Enterobacteriaceae Reference Laboratories, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA (d)
Author Notes
* ↵* Present address: Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada.
1. Address correspondence to Yan Boucher, yboucher@ualberta.ca, or Martin F. Polz, mpolz@mit.edu.
1. Editor David Relman, VA Palo Alto Health Care System
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.
Footnotes
* Citation Boucher Y, et al. 2011. Local mobile gene pools rapidly cross species boundaries to create endemicity within global Vibrio cholerae populations. mBio 2(2):e00335-10. doi:10.1128/mBio.00335-10.
* Received 18 December 2010
* Accepted 22 March 2011
* Published 12 April 2011
* Copyright ? 2011 Boucher et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
-
-----