Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria

ABSTRACT Metazoans were proposed to host bacteriophages on their mucosal surfaces in a symbiotic relationship, where phages provide an external immunity against bacterial infections and the metazoans provide phages a medium for interacting with bacteria. However, scarce empirical evidence and model...

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Autores principales:	Gabriel M. F. Almeida, Elina Laanto, Roghaieh Ashrafi, Lotta-Riina Sundberg
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	bacterial virulence bacteriophage therapy bacteriophages host-pathogen interactions mucosal pathogens Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/4d557f0fd5d64bf78f54af0e4d6dcdfd
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spelling	oai:doaj.org-article:4d557f0fd5d64bf78f54af0e4d6dcdfd2021-11-15T15:54:47ZBacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria10.1128/mBio.01984-192150-7511https://doaj.org/article/4d557f0fd5d64bf78f54af0e4d6dcdfd2019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01984-19https://doaj.org/toc/2150-7511ABSTRACT Metazoans were proposed to host bacteriophages on their mucosal surfaces in a symbiotic relationship, where phages provide an external immunity against bacterial infections and the metazoans provide phages a medium for interacting with bacteria. However, scarce empirical evidence and model systems have left the phage-mucus interaction poorly understood. Here, we show that phages bind both to porcine mucus and to rainbow trout (Oncorhynchus mykiss) primary mucus, persist up to 7 days in the mucosa, and provide protection against Flavobacterium columnare. Also, exposure to mucus changes the bacterial phenotype by increasing bacterial virulence and susceptibility to phage infections. This trade-off in bacterial virulence reveals ecological benefit of maintaining phages in the metazoan mucosal surfaces. Tests using other phage-bacterium pairs suggest that phage binding to mucus may be widespread in the biosphere, indicating its importance for disease, ecology, and evolution. This phenomenon may have significant potential to be exploited in preventive phage therapy. IMPORTANCE The mucosal surfaces of animals are habitat for microbes, including viruses. Bacteriophages—viruses that infect bacteria—were shown to be able to bind to mucus. This may result in a symbiotic relationship in which phages find bacterial hosts to infect, protecting the mucus-producing animal from bacterial infections in the process. Here, we studied phage binding on mucus and the effect of mucin on phage-bacterium interactions. The significance of our research is in showing that phage adhesion to mucus results in preventive protection against bacterial infections, which will serve as basis for the development of prophylactic phage therapy approaches. Besides, we also reveal that exposure to mucus upregulates bacterial virulence and that this is exploited by phages for infection, adding one additional layer to the metazoan-bacterium-phage biological interactions and ecology. This phenomenon might be widespread in the biosphere and thus crucial for understanding mucosal diseases, their outcome and treatment.Gabriel M. F. AlmeidaElina LaantoRoghaieh AshrafiLotta-Riina SundbergAmerican Society for Microbiologyarticlebacterial virulencebacteriophage therapybacteriophageshost-pathogen interactionsmucosal pathogensMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacterial virulence bacteriophage therapy bacteriophages host-pathogen interactions mucosal pathogens Microbiology QR1-502
spellingShingle	bacterial virulence bacteriophage therapy bacteriophages host-pathogen interactions mucosal pathogens Microbiology QR1-502 Gabriel M. F. Almeida Elina Laanto Roghaieh Ashrafi Lotta-Riina Sundberg Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria
description	ABSTRACT Metazoans were proposed to host bacteriophages on their mucosal surfaces in a symbiotic relationship, where phages provide an external immunity against bacterial infections and the metazoans provide phages a medium for interacting with bacteria. However, scarce empirical evidence and model systems have left the phage-mucus interaction poorly understood. Here, we show that phages bind both to porcine mucus and to rainbow trout (Oncorhynchus mykiss) primary mucus, persist up to 7 days in the mucosa, and provide protection against Flavobacterium columnare. Also, exposure to mucus changes the bacterial phenotype by increasing bacterial virulence and susceptibility to phage infections. This trade-off in bacterial virulence reveals ecological benefit of maintaining phages in the metazoan mucosal surfaces. Tests using other phage-bacterium pairs suggest that phage binding to mucus may be widespread in the biosphere, indicating its importance for disease, ecology, and evolution. This phenomenon may have significant potential to be exploited in preventive phage therapy. IMPORTANCE The mucosal surfaces of animals are habitat for microbes, including viruses. Bacteriophages—viruses that infect bacteria—were shown to be able to bind to mucus. This may result in a symbiotic relationship in which phages find bacterial hosts to infect, protecting the mucus-producing animal from bacterial infections in the process. Here, we studied phage binding on mucus and the effect of mucin on phage-bacterium interactions. The significance of our research is in showing that phage adhesion to mucus results in preventive protection against bacterial infections, which will serve as basis for the development of prophylactic phage therapy approaches. Besides, we also reveal that exposure to mucus upregulates bacterial virulence and that this is exploited by phages for infection, adding one additional layer to the metazoan-bacterium-phage biological interactions and ecology. This phenomenon might be widespread in the biosphere and thus crucial for understanding mucosal diseases, their outcome and treatment.
format	article
author	Gabriel M. F. Almeida Elina Laanto Roghaieh Ashrafi Lotta-Riina Sundberg
author_facet	Gabriel M. F. Almeida Elina Laanto Roghaieh Ashrafi Lotta-Riina Sundberg
author_sort	Gabriel M. F. Almeida
title	Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria
title_short	Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria
title_full	Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria
title_fullStr	Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria
title_full_unstemmed	Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria
title_sort	bacteriophage adherence to mucus mediates preventive protection against pathogenic bacteria
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/4d557f0fd5d64bf78f54af0e4d6dcdfd
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Bacteriophage Adherence to Mucus Mediates Preventive Protection against Pathogenic Bacteria

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