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Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1

Bacteriophages are highly abundant in human microbiota where they coevolve with resident bacteria. Phage predation can drive the evolution of bacterial resistance, which can then drive reciprocal evolution in the phage to overcome that resistance. Such coevolutionary dynamics have not been extensive...

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Autores principales: Wandro, Stephen, Oliver, Andrew, Gallagher, Tara, Weihe, Claudia, England, Whitney, Martiny, Jennifer B. H., Whiteson, Katrine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6365445/
https://www.ncbi.nlm.nih.gov/pubmed/30766528
http://dx.doi.org/10.3389/fmicb.2018.03192
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author Wandro, Stephen
Oliver, Andrew
Gallagher, Tara
Weihe, Claudia
England, Whitney
Martiny, Jennifer B. H.
Whiteson, Katrine
author_facet Wandro, Stephen
Oliver, Andrew
Gallagher, Tara
Weihe, Claudia
England, Whitney
Martiny, Jennifer B. H.
Whiteson, Katrine
author_sort Wandro, Stephen
collection PubMed
description Bacteriophages are highly abundant in human microbiota where they coevolve with resident bacteria. Phage predation can drive the evolution of bacterial resistance, which can then drive reciprocal evolution in the phage to overcome that resistance. Such coevolutionary dynamics have not been extensively studied in human gut bacteria, and are of particular interest for both understanding and eventually manipulating the human gut microbiome. We performed experimental evolution of an Enterococcus faecium isolate from healthy human stool in the absence and presence of a single infecting Myoviridae bacteriophage, EfV12-phi1. Four replicates of E. faecium and phage were grown with twice daily serial transfers for 8 days. Genome sequencing revealed that E. faecium evolved resistance to phage through mutations in the yqwD2 gene involved in exopolysaccharide biogenesis and export, and the rpoC gene which encodes the RNA polymerase β’ subunit. In response to bacterial resistance, phage EfV12-phi1 evolved varying numbers of 1.8 kb tandem duplications within a putative tail fiber gene. Host range assays indicated that coevolution of this phage-host pair resulted in arms race dynamics in which bacterial resistance and phage infectivity increased over time. Tracking mutations from population sequencing of experimental coevolution can quickly illuminate phage entry points along with resistance strategies in both phage and host – critical information for using phage to manipulate microbial communities.
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spelling pubmed-63654452019-02-14 Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1 Wandro, Stephen Oliver, Andrew Gallagher, Tara Weihe, Claudia England, Whitney Martiny, Jennifer B. H. Whiteson, Katrine Front Microbiol Microbiology Bacteriophages are highly abundant in human microbiota where they coevolve with resident bacteria. Phage predation can drive the evolution of bacterial resistance, which can then drive reciprocal evolution in the phage to overcome that resistance. Such coevolutionary dynamics have not been extensively studied in human gut bacteria, and are of particular interest for both understanding and eventually manipulating the human gut microbiome. We performed experimental evolution of an Enterococcus faecium isolate from healthy human stool in the absence and presence of a single infecting Myoviridae bacteriophage, EfV12-phi1. Four replicates of E. faecium and phage were grown with twice daily serial transfers for 8 days. Genome sequencing revealed that E. faecium evolved resistance to phage through mutations in the yqwD2 gene involved in exopolysaccharide biogenesis and export, and the rpoC gene which encodes the RNA polymerase β’ subunit. In response to bacterial resistance, phage EfV12-phi1 evolved varying numbers of 1.8 kb tandem duplications within a putative tail fiber gene. Host range assays indicated that coevolution of this phage-host pair resulted in arms race dynamics in which bacterial resistance and phage infectivity increased over time. Tracking mutations from population sequencing of experimental coevolution can quickly illuminate phage entry points along with resistance strategies in both phage and host – critical information for using phage to manipulate microbial communities. Frontiers Media S.A. 2019-01-31 /pmc/articles/PMC6365445/ /pubmed/30766528 http://dx.doi.org/10.3389/fmicb.2018.03192 Text en Copyright © 2019 Wandro, Oliver, Gallagher, Weihe, England, Martiny and Whiteson. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Wandro, Stephen
Oliver, Andrew
Gallagher, Tara
Weihe, Claudia
England, Whitney
Martiny, Jennifer B. H.
Whiteson, Katrine
Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1
title Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1
title_full Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1
title_fullStr Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1
title_full_unstemmed Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1
title_short Predictable Molecular Adaptation of Coevolving Enterococcus faecium and Lytic Phage EfV12-phi1
title_sort predictable molecular adaptation of coevolving enterococcus faecium and lytic phage efv12-phi1
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6365445/
https://www.ncbi.nlm.nih.gov/pubmed/30766528
http://dx.doi.org/10.3389/fmicb.2018.03192
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