Using a human colonoid-derived monolayer to study bacteriophage translocation

Gut Microbes. 2024 Jan-Dec;16(1):2331520. doi: 10.1080/19490976.2024.2331520. Epub 2024 Mar 22.

Abstract

Bacteriophages (phages) are estimated to be the most abundant microorganisms on Earth. Their presence in human blood suggests that they can translocate from non-sterile sites such as the gastrointestinal tract where they are concentrated. To examine phage translocation ex vivo, we adapted a primary colonoid monolayer model possessing cell diversity and architecture, and a thick layer of mucus akin to the colonic environment in vivo. We show that the colonoid monolayer is superior to the Caco-2 cell-line model, possessing intact and organized tight junctions and generating a physiologically relevant mucus layer. We showed, using two different phages, that translocation across the colonoid monolayer was largely absent in differentiated monolayers that express mucus, unlike Caco-2 cultures that expressed little to no mucus. By stimulating mucus production or removing mucus, we further demonstrated the importance of colonic mucus in preventing phage translocation. Finally, we used etiological drivers of gut permeability (alcohol, fat, and inflammatory cytokines) to measure their effects on phage translocation, demonstrating that all three stimuli have the capacity to amplify phage translocation. These findings suggest that phage translocation does occur in vivo but may be largely dependent on colonic mucus, an important insight to consider in future phage applications.

Keywords: Bacteriophage; colonoid; intestinal permeability; phage therapy; translocation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bacteriophages* / physiology
  • Caco-2 Cells
  • Colon
  • Gastrointestinal Microbiome*
  • Humans
  • Tight Junctions

Grants and funding

The work was supported by the National Health and Medical Research Council Thyne Reid Foundation Ainsworth Bequest Robert W. Storr Bequest Early-Mid Career Phage Therapy grants (Office for Health and Medical Research; Ministry of Health, New South Wales; Australia MRFF Frontiers Stage 1).