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Rapid evolution of microbe-mediated protection against pathogens in a worm host

Microbes can defend their host against virulent infections, but direct evidence for the adaptive origin of microbe-mediated protection is lacking. Using experimental evolution of a novel, tripartite interaction, we demonstrate that mildly pathogenic bacteria (Enterococcus faecalis) living in worms (...

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Autores principales: King, Kayla C, Brockhurst, Michael A, Vasieva, Olga, Paterson, Steve, Betts, Alex, Ford, Suzanne A, Frost, Crystal L, Horsburgh, Malcolm J, Haldenby, Sam, Hurst, Gregory DD
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5029159/
https://www.ncbi.nlm.nih.gov/pubmed/26978164
http://dx.doi.org/10.1038/ismej.2015.259
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author King, Kayla C
Brockhurst, Michael A
Vasieva, Olga
Paterson, Steve
Betts, Alex
Ford, Suzanne A
Frost, Crystal L
Horsburgh, Malcolm J
Haldenby, Sam
Hurst, Gregory DD
author_facet King, Kayla C
Brockhurst, Michael A
Vasieva, Olga
Paterson, Steve
Betts, Alex
Ford, Suzanne A
Frost, Crystal L
Horsburgh, Malcolm J
Haldenby, Sam
Hurst, Gregory DD
author_sort King, Kayla C
collection PubMed
description Microbes can defend their host against virulent infections, but direct evidence for the adaptive origin of microbe-mediated protection is lacking. Using experimental evolution of a novel, tripartite interaction, we demonstrate that mildly pathogenic bacteria (Enterococcus faecalis) living in worms (Caenorhabditis elegans) rapidly evolved to defend their animal hosts against infection by a more virulent pathogen (Staphylococcus aureus), crossing the parasitism–mutualism continuum. Host protection evolved in all six, independently selected populations in response to within-host bacterial interactions and without direct selection for host health. Microbe-mediated protection was also effective against a broad spectrum of pathogenic S. aureus isolates. Genomic analysis implied that the mechanistic basis for E. faecalis-mediated protection was through increased production of antimicrobial superoxide, which was confirmed by biochemical assays. Our results indicate that microbes living within a host may make the evolutionary transition to mutualism in response to pathogen attack, and that microbiome evolution warrants consideration as a driver of infection outcome.
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spelling pubmed-50291592016-09-21 Rapid evolution of microbe-mediated protection against pathogens in a worm host King, Kayla C Brockhurst, Michael A Vasieva, Olga Paterson, Steve Betts, Alex Ford, Suzanne A Frost, Crystal L Horsburgh, Malcolm J Haldenby, Sam Hurst, Gregory DD ISME J Original Article Microbes can defend their host against virulent infections, but direct evidence for the adaptive origin of microbe-mediated protection is lacking. Using experimental evolution of a novel, tripartite interaction, we demonstrate that mildly pathogenic bacteria (Enterococcus faecalis) living in worms (Caenorhabditis elegans) rapidly evolved to defend their animal hosts against infection by a more virulent pathogen (Staphylococcus aureus), crossing the parasitism–mutualism continuum. Host protection evolved in all six, independently selected populations in response to within-host bacterial interactions and without direct selection for host health. Microbe-mediated protection was also effective against a broad spectrum of pathogenic S. aureus isolates. Genomic analysis implied that the mechanistic basis for E. faecalis-mediated protection was through increased production of antimicrobial superoxide, which was confirmed by biochemical assays. Our results indicate that microbes living within a host may make the evolutionary transition to mutualism in response to pathogen attack, and that microbiome evolution warrants consideration as a driver of infection outcome. Nature Publishing Group 2016-08 2016-03-15 /pmc/articles/PMC5029159/ /pubmed/26978164 http://dx.doi.org/10.1038/ismej.2015.259 Text en Copyright © 2016 International Society for Microbial Ecology http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Original Article
King, Kayla C
Brockhurst, Michael A
Vasieva, Olga
Paterson, Steve
Betts, Alex
Ford, Suzanne A
Frost, Crystal L
Horsburgh, Malcolm J
Haldenby, Sam
Hurst, Gregory DD
Rapid evolution of microbe-mediated protection against pathogens in a worm host
title Rapid evolution of microbe-mediated protection against pathogens in a worm host
title_full Rapid evolution of microbe-mediated protection against pathogens in a worm host
title_fullStr Rapid evolution of microbe-mediated protection against pathogens in a worm host
title_full_unstemmed Rapid evolution of microbe-mediated protection against pathogens in a worm host
title_short Rapid evolution of microbe-mediated protection against pathogens in a worm host
title_sort rapid evolution of microbe-mediated protection against pathogens in a worm host
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5029159/
https://www.ncbi.nlm.nih.gov/pubmed/26978164
http://dx.doi.org/10.1038/ismej.2015.259
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