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Capturing dynamic phage-pathogen coevolution by clinical surveillance.

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Bacteria and viruses engage in a constant evolutionary battle. A new mobile genetic element, PLE11, emerged in Vibrio cholerae, driving pathogen evolution during a major cholera outbreak by targeting the ICP1 phage.

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Area of Science:

  • Microbiology
  • Evolutionary Biology
  • Genetics

Background:

  • Bacteria possess defense systems against phage predation, often encoded on mobile genetic elements.
  • Bacteriophages (phages) and bacteria engage in a dynamic evolutionary arms race, particularly relevant in human diseases.
  • In Vibrio cholerae, higher ICP1 phage loads correlate with reduced diarrheal disease severity, but direct evidence of phage-driven bacterial selection was lacking.

Purpose of the Study:

  • To investigate the molecular mechanisms driving the natural selection of the globally important pathogen Vibrio cholerae.
  • To understand the evolutionary dynamics between Vibrio cholerae and its lytic phage ICP1 in a clinical context.
  • To identify the genetic basis for the emergence and dominance of anti-phage elements during a cholera outbreak.

Main Methods:

  • Clinical surveillance in cholera-endemic Bangladesh to identify mobile genetic elements.
  • Experimental evolution to study phage counter-adaptations.
  • Molecular characterization of the anti-phage mechanism and phage-host interactions.
  • Analysis of mobile genetic element (PLE) and phage (ICP1) genome sequences.

Main Results:

  • The acquisition of a parasitic anti-phage mobile genetic element, PLE11, coincided with a major Vibrio cholerae outbreak.
  • PLE11 exhibited potent anti-phage activity against ICP1, mediated by the Rta protein, which restricts phage tail assembly.
  • Experimental evolution revealed phage counter-adaptations, leading to the emergence of ICP1 variants capable of overcoming PLE11.
  • PLEs were found to construct chimeric tails for horizontal transmission, balancing defense with propagation.

Conclusions:

  • The study reveals the molecular basis for the natural selection of Vibrio cholerae, driven by phage predation and mobile genetic element-mediated defense.
  • PLE11's emergence and selection demonstrate a rapid evolutionary response to phage pressure in a clinically relevant pathogen.
  • The findings highlight the complex interplay between bacteria, phages, and mobile genetic elements in shaping pathogen evolution during disease outbreaks.