Evolutionary consequences of intra-patient phage predation on microbial populations

The impact of phage predation on bacterial pathogens in the context of human disease is not currently appreciated. Here, we show that predatory interactions of a phage with an important environmentally transmitted pathogen, Vibrio cholerae, can modulate the evolutionary trajectory of this pathogen d...

Full description

Bibliographic Details
Main Authors: Kimberley D Seed, Minmin Yen, B Jesse Shapiro, Isabelle J Hilaire, Richelle C Charles, Jessica E Teng, Louise C Ivers, Jacques Boncy, Jason B Harris, Andrew Camilli
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2014-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/03497
_version_ 1811235862170566656
author Kimberley D Seed
Minmin Yen
B Jesse Shapiro
Isabelle J Hilaire
Richelle C Charles
Jessica E Teng
Louise C Ivers
Jacques Boncy
Jason B Harris
Andrew Camilli
author_facet Kimberley D Seed
Minmin Yen
B Jesse Shapiro
Isabelle J Hilaire
Richelle C Charles
Jessica E Teng
Louise C Ivers
Jacques Boncy
Jason B Harris
Andrew Camilli
author_sort Kimberley D Seed
collection DOAJ
description The impact of phage predation on bacterial pathogens in the context of human disease is not currently appreciated. Here, we show that predatory interactions of a phage with an important environmentally transmitted pathogen, Vibrio cholerae, can modulate the evolutionary trajectory of this pathogen during the natural course of infection within individual patients. We analyzed geographically and temporally disparate cholera patient stool samples from Haiti and Bangladesh and found that phage predation can drive the genomic diversity of intra-patient V. cholerae populations. Intra-patient phage-sensitive and phage-resistant isolates were isogenic except for mutations conferring phage resistance, and moreover, phage-resistant V. cholerae populations were composed of a heterogeneous mix of many unique mutants. We also observed that phage predation can significantly alter the virulence potential of V. cholerae shed from cholera patients. We provide the first molecular evidence for predatory phage shaping microbial community structure during the natural course of infection in humans.
first_indexed 2024-04-12T11:59:22Z
format Article
id doaj.art-a80bbcce4b904e378dbe1e2c2d25f265
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-12T11:59:22Z
publishDate 2014-08-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-a80bbcce4b904e378dbe1e2c2d25f2652022-12-22T03:33:53ZengeLife Sciences Publications LtdeLife2050-084X2014-08-01310.7554/eLife.03497Evolutionary consequences of intra-patient phage predation on microbial populationsKimberley D Seed0Minmin Yen1B Jesse Shapiro2Isabelle J Hilaire3Richelle C Charles4Jessica E Teng5Louise C Ivers6Jacques Boncy7Jason B Harris8Andrew Camilli9Department of Molecular Biology and Microbiology, Howard Hughes Medical Institute, Tufts University School of Medicine, Boston, United StatesDepartment of Molecular Biology and Microbiology, Howard Hughes Medical Institute, Tufts University School of Medicine, Boston, United StatesDépartement de sciences biologiques, Université de Montréal, Montreal, CanadaPartners In Health, Boston, United StatesDivision of Infectious Diseases, Massachusetts General Hospital, Boston, United States; Department of Medicine, Harvard Medical School, Boston, United StatesPartners In Health, Boston, United States; Division of Global Health Equity, Brigham and Women's Hospital, Boston, United StatesPartners In Health, Boston, United States; Division of Global Health Equity, Brigham and Women's Hospital, Boston, United States; Department of Global Health and Social Medicine, Harvard Medical School, Boston, United StatesNational Public Health Laboratory, Port-au-Prince, HaitiDivision of Infectious Diseases, Massachusetts General Hospital, Boston, United States; Department of Medicine, Harvard Medical School, Boston, United States; Department of Pediatrics, Harvard Medical School, Boston, United StatesDepartment of Molecular Biology and Microbiology, Howard Hughes Medical Institute, Tufts University School of Medicine, Boston, United StatesThe impact of phage predation on bacterial pathogens in the context of human disease is not currently appreciated. Here, we show that predatory interactions of a phage with an important environmentally transmitted pathogen, Vibrio cholerae, can modulate the evolutionary trajectory of this pathogen during the natural course of infection within individual patients. We analyzed geographically and temporally disparate cholera patient stool samples from Haiti and Bangladesh and found that phage predation can drive the genomic diversity of intra-patient V. cholerae populations. Intra-patient phage-sensitive and phage-resistant isolates were isogenic except for mutations conferring phage resistance, and moreover, phage-resistant V. cholerae populations were composed of a heterogeneous mix of many unique mutants. We also observed that phage predation can significantly alter the virulence potential of V. cholerae shed from cholera patients. We provide the first molecular evidence for predatory phage shaping microbial community structure during the natural course of infection in humans.https://elifesciences.org/articles/03497Vibrio choleraecholerabacteriophagephageOmpUToxR
spellingShingle Kimberley D Seed
Minmin Yen
B Jesse Shapiro
Isabelle J Hilaire
Richelle C Charles
Jessica E Teng
Louise C Ivers
Jacques Boncy
Jason B Harris
Andrew Camilli
Evolutionary consequences of intra-patient phage predation on microbial populations
eLife
Vibrio cholerae
cholera
bacteriophage
phage
OmpU
ToxR
title Evolutionary consequences of intra-patient phage predation on microbial populations
title_full Evolutionary consequences of intra-patient phage predation on microbial populations
title_fullStr Evolutionary consequences of intra-patient phage predation on microbial populations
title_full_unstemmed Evolutionary consequences of intra-patient phage predation on microbial populations
title_short Evolutionary consequences of intra-patient phage predation on microbial populations
title_sort evolutionary consequences of intra patient phage predation on microbial populations
topic Vibrio cholerae
cholera
bacteriophage
phage
OmpU
ToxR
url https://elifesciences.org/articles/03497
work_keys_str_mv AT kimberleydseed evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT minminyen evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT bjesseshapiro evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT isabellejhilaire evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT richelleccharles evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT jessicaeteng evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT louisecivers evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT jacquesboncy evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT jasonbharris evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations
AT andrewcamilli evolutionaryconsequencesofintrapatientphagepredationonmicrobialpopulations