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T4 Bacteriophage and E. coli Interaction in the Murine Intestine: A Prototypical Model for Studying Host-Bacteriophage Dynamics In Vivo
Published on: January 26, 2024
Bacteriophage adhering to mucus provide a non-host-derived immunity
Jeremy J Barr1, Rita Auro, Mike Furlan
1Department of Biology, San Diego State University, San Diego, CA 92182, USA. jeremybarr85@gmail.com
Abstract:
Mucosal surfaces are a main entry point for pathogens and the principal sites of defense against infection. Both bacteria and phage are associated with this mucus. Here we show that phage-to-bacteria ratios were increased, relative to the adjacent environment, on all mucosal surfaces sampled, ranging from cnidarians to humans. In vitro studies of tissue culture cells with and without surface mucus demonstrated that this increase in phage abundance is mucus dependent and protects the underlying epithelium from bacterial infection. Enrichment of phage in mucus occurs via binding interactions between mucin glycoproteins and Ig-like protein domains exposed on phage capsids. In particular, phage Ig-like domains bind variable glycan residues that coat the mucin glycoprotein component of mucus. Metagenomic analysis found these Ig-like proteins present in the phages sampled from many environments, particularly from locations adjacent to mucosal surfaces. Based on these observations, we present the bacteriophage adherence to mucus model that provides a ubiquitous, but non-host-derived, immunity applicable to mucosal surfaces. The model suggests that metazoan mucosal surfaces and phage coevolve to maintain phage adherence. This benefits the metazoan host by limiting mucosal bacteria, and benefits the phage through more frequent interactions with bacterial hosts. The relationships shown here suggest a symbiotic relationship between phage and metazoan hosts that provides a previously unrecognized antimicrobial defense that actively protects mucosal surfaces.
Insights
Bacteriophages (phage) are enriched in mucus on mucosal surfaces, providing a mucus-dependent defense against bacterial infection. This natural, symbiotic relationship offers a previously unrecognized form of innate immunity for metazoan hosts.
Area of Science:
- Microbiology
- Immunology
- Evolutionary Biology
Background:
- Mucosal surfaces are critical interfaces for host-pathogen interactions and immune defense.
- Bacteria and bacteriophages (phage) are commonly found associated with mucus layers.
- The ecological dynamics and functional roles of phages in mucosal environments remain incompletely understood.
Purpose of the Study:
- To investigate the abundance and distribution of phages on various mucosal surfaces.
- To determine the role of mucus in phage enrichment and its impact on bacterial colonization.
- To elucidate the molecular mechanisms underlying phage-mucus interactions and their ecological implications.
Main Methods:
- Comparative analysis of phage-to-bacteria ratios across diverse mucosal surfaces (cnidarians to humans).
- In vitro studies using tissue culture cells with and without mucus to assess phage-dependent protection against bacterial infection.
- Biochemical analysis of phage-mucin interactions, focusing on phage capsid proteins and mucus glycoproteins.
- Metagenomic analysis of phage populations to identify relevant protein domains.
Main Results:
- Phage-to-bacteria ratios were significantly higher on mucosal surfaces compared to adjacent environments.
- Phage enrichment in mucus was demonstrated to be mucus-dependent and conferred protection to underlying epithelial cells from bacterial infection.
- Phage Ig-like protein domains were identified as key mediators of binding to mucin glycoproteins via specific glycan residues.
- Metagenomic data revealed the prevalence of these Ig-like domains in phages from diverse environments, especially near mucosal surfaces.
Conclusions:
- The bacteriophage adherence to mucus (BAM) model proposes a ubiquitous, non-host-derived immunity mechanism for mucosal surfaces.
- Co-evolution between metazoan mucosal surfaces and phages promotes phage adherence, benefiting hosts by limiting bacteria and phages through enhanced host interaction.
- A symbiotic relationship exists between phage and metazoan hosts, establishing a novel antimicrobial defense system for mucosal surfaces.
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