Vibrio cholerae residing in food vacuoles expelled by protozoa are more infectious in vivo

Nat Microbiol. 2019 Dec;4(12):2466-2474. doi: 10.1038/s41564-019-0563-x. Epub 2019 Sep 30.

Abstract

Vibrio cholerae interacts with many organisms in the environment, including heterotrophic protists (protozoa). Several species of protozoa have been reported to release undigested bacteria in expelled food vacuoles (EFVs) when feeding on some pathogens. While the production of EFVs has been reported, their biological role as a vector for the transmission of pathogens remains unknown. Here we report that ciliated protozoa release EFVs containing V. cholerae. The EFVs are stable, the cells inside them are protected from multiple stresses, and large numbers of cells escape when incubated at 37 °C or in the presence of nutrients. We show that OmpU, a major outer membrane protein positively regulated by ToxR, has a role in the production of EFVs. Notably, cells released from EFVs have growth and colonization advantages over planktonic cells both in vitro and in vivo. Our results suggest that EFVs facilitate V. cholerae survival in the environment, enhancing their infectious potential and may contribute to the dissemination of epidemic V. cholerae strains. These results improve our understanding of the mechanisms of persistence and the modes of transmission of V. cholerae and may further apply to other opportunistic pathogens that have been shown to be released by protists in EFVs.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adhesins, Bacterial / metabolism
  • Animals
  • Bacterial Outer Membrane Proteins
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cholera / microbiology*
  • Cholera / parasitology
  • Cholera / transmission
  • Communicable Diseases / microbiology
  • Communicable Diseases / parasitology
  • DNA-Binding Proteins
  • Disease Models, Animal
  • Disease Vectors*
  • Female
  • Host-Pathogen Interactions / physiology*
  • Male
  • Mice
  • Temperature
  • Tetrahymena pyriformis / microbiology*
  • Transcription Factors
  • Vacuoles / microbiology*
  • Vacuoles / parasitology
  • Vibrio cholerae / genetics
  • Vibrio cholerae / growth & development*
  • Vibrio cholerae / metabolism*

Substances

  • Adhesins, Bacterial
  • Bacterial Outer Membrane Proteins
  • Bacterial Proteins
  • DNA-Binding Proteins
  • OmpU protein, Vibrio cholerae
  • Transcription Factors
  • toxR protein, Vibrio cholerae