Niche adaptation limits bacteriophage predation of Vibrio cholerae in a nutrient-poor aquatic environment

Andrew Camilli,Cecilia A. Silva-Valenzuela

doi:10.1073/pnas.1810138116

Andrew Camilli, Cecilia A. Silva-Valenzuela

Open Access

https://doi.org/10.1073/pnas.1810138116

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Abstract

Vibrio cholerae, the causative agent of cholera, has reservoirs in fresh and brackish water where it interacts with virulent bacteriophages. Phages are the most abundant biological entity on earth and coevolve with bacteria. It was reported that concentrations of phage and V. cholerae inversely correlate in aquatic reservoirs and in the human small intestine, and therefore that phages may quench cholera outbreaks. Although there is strong evidence for phage predation in cholera patients, evidence is lacking for phage predation of V. cholerae in aquatic environments. Here, we used three virulent phages, ICP1, ICP2, and ICP3, commonly shed by cholera patients in Bangladesh, as models to understand the predation dynamics in microcosms simulating aquatic environments. None of the phages were capable of predation in fresh water, and only ICP1 was able to prey on V. cholerae in estuarine water due to a requirement for salt. We conclude that ICP2 and ICP3 are better adapted for predation in a nutrient rich environment. Our results point to the evolution of niche-specific predation by V. cholerae-specific virulent phages, which complicates their use in predicting or monitoring cholera outbreaks as well as their potential use in reducing aquatic reservoirs of V. cholerae in endemic areas.

Highlights

The water-borne bacterium Vibrio cholerae causes cholera, an acute intestinal infection characterized by profuse secretory diarrhea that can quickly lead to severe dehydration and death if untreated
Together the results suggest that: (i) ICP1 can kill V. cholerae and replicate in a higher salinity condition than the one found in fresh water, (ii) only a small number of ICP2 phages replicate in V. cholerae in an estuary environment, and (iii) infection by ICP3 is unsuccessful in both aquatic environments
Our results have relevance for understanding the impact of virulent phages on V. cholerae during cholera outbreaks during which V. cholerae and phages are shed in secretory diarrhea into bodies of water and are subsequently transmitted via consumption of contaminated fresh water

Summary

Introduction

The water-borne bacterium Vibrio cholerae causes cholera, an acute intestinal infection characterized by profuse secretory diarrhea that can quickly lead to severe dehydration and death if untreated. This pathogen is able to persist in aquatic environments in planktonic form or by association with phytoplankton and the chitinous carapaces of zooplankton [1] and is endemic in many countries where it forms reservoirs in fresh water and estuarine environments [2]. ICP1 can replicate in V. cholerae in fresh water that is supplemented with NaCl, salinity could be a critical variable in relation to environmental phage predation

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