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

TY - JOUR

T1 - Rapid evolution of microbe-mediated protection against pathogens in a worm host

AU - King, Kayla C

AU - Brockhurst, Michael A

AU - Vasieva, Olga

AU - Paterson, Steve

AU - Betts, Alex

AU - Ford, Suzanne A

AU - Frost, Crystal L

AU - Horsburgh, Malcolm J

AU - Haldenby, Sam

AU - Hurst, Gregory DD

N1 - © 2016 International Society for Microbial Ecology

PY - 2016/3/15

Y1 - 2016/3/15

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=84961219421&partnerID=8YFLogxK

U2 - 10.1038/ismej.2015.259

DO - 10.1038/ismej.2015.259

M3 - Article

C2 - 26978164

SN - 1751-7362

VL - 10

SP - 1915

EP - 1924

JO - The ISME Journal

JF - The ISME Journal

IS - 8

ER -