Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.

The health and environmental risks associated with antibiotic use in aquaculture have promoted bacterial probiotics as an alternative approach to control fish infections in vulnerable larval and juvenile stages. However, evidence-based identification of probiotics is often hindered by the complexity...

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Main Authors: David Pérez-Pascual, Sol Vendrell-Fernández, Bianca Audrain, Joaquín Bernal-Bayard, Rafael Patiño-Navarrete, Vincent Petit, Dimitri Rigaudeau, Jean-Marc Ghigo
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS Pathogens
Online Access:https://doi.org/10.1371/journal.ppat.1009302
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spelling doaj-d34c7b2734004ae386dc62f95c4033f12021-05-15T04:31:00ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742021-01-01171e100930210.1371/journal.ppat.1009302Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.David Pérez-PascualSol Vendrell-FernándezBianca AudrainJoaquín Bernal-BayardRafael Patiño-NavarreteVincent PetitDimitri RigaudeauJean-Marc GhigoThe health and environmental risks associated with antibiotic use in aquaculture have promoted bacterial probiotics as an alternative approach to control fish infections in vulnerable larval and juvenile stages. However, evidence-based identification of probiotics is often hindered by the complexity of bacteria-host interactions and host variability in microbiologically uncontrolled conditions. While these difficulties can be partially resolved using gnotobiotic models harboring no or reduced microbiota, most host-microbe interaction studies are carried out in animal models with little relevance for fish farming. Here we studied host-microbiota-pathogen interactions in a germ-free and gnotobiotic model of rainbow trout (Oncorhynchus mykiss), one of the most widely cultured salmonids. We demonstrated that germ-free larvae raised in sterile conditions displayed no significant difference in growth after 35 days compared to conventionally-raised larvae, but were extremely sensitive to infection by Flavobacterium columnare, a common freshwater fish pathogen causing major economic losses worldwide. Furthermore, re-conventionalization with 11 culturable species from the conventional trout microbiota conferred resistance to F. columnare infection. Using mono-re-conventionalized germ-free trout, we identified that this protection is determined by a commensal Flavobacterium strain displaying antibacterial activity against F. columnare. Finally, we demonstrated that use of gnotobiotic trout is a suitable approach for the identification of both endogenous and exogenous probiotic bacterial strains protecting teleostean hosts against F. columnare. This study therefore establishes an ecologically-relevant gnotobiotic model for the study of host-pathogen interactions and colonization resistance in farmed fish.https://doi.org/10.1371/journal.ppat.1009302
collection DOAJ
language English
format Article
sources DOAJ
author David Pérez-Pascual
Sol Vendrell-Fernández
Bianca Audrain
Joaquín Bernal-Bayard
Rafael Patiño-Navarrete
Vincent Petit
Dimitri Rigaudeau
Jean-Marc Ghigo
spellingShingle David Pérez-Pascual
Sol Vendrell-Fernández
Bianca Audrain
Joaquín Bernal-Bayard
Rafael Patiño-Navarrete
Vincent Petit
Dimitri Rigaudeau
Jean-Marc Ghigo
Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.
PLoS Pathogens
author_facet David Pérez-Pascual
Sol Vendrell-Fernández
Bianca Audrain
Joaquín Bernal-Bayard
Rafael Patiño-Navarrete
Vincent Petit
Dimitri Rigaudeau
Jean-Marc Ghigo
author_sort David Pérez-Pascual
title Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.
title_short Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.
title_full Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.
title_fullStr Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.
title_full_unstemmed Gnotobiotic rainbow trout (Oncorhynchus mykiss) model reveals endogenous bacteria that protect against Flavobacterium columnare infection.
title_sort gnotobiotic rainbow trout (oncorhynchus mykiss) model reveals endogenous bacteria that protect against flavobacterium columnare infection.
publisher Public Library of Science (PLoS)
series PLoS Pathogens
issn 1553-7366
1553-7374
publishDate 2021-01-01
description The health and environmental risks associated with antibiotic use in aquaculture have promoted bacterial probiotics as an alternative approach to control fish infections in vulnerable larval and juvenile stages. However, evidence-based identification of probiotics is often hindered by the complexity of bacteria-host interactions and host variability in microbiologically uncontrolled conditions. While these difficulties can be partially resolved using gnotobiotic models harboring no or reduced microbiota, most host-microbe interaction studies are carried out in animal models with little relevance for fish farming. Here we studied host-microbiota-pathogen interactions in a germ-free and gnotobiotic model of rainbow trout (Oncorhynchus mykiss), one of the most widely cultured salmonids. We demonstrated that germ-free larvae raised in sterile conditions displayed no significant difference in growth after 35 days compared to conventionally-raised larvae, but were extremely sensitive to infection by Flavobacterium columnare, a common freshwater fish pathogen causing major economic losses worldwide. Furthermore, re-conventionalization with 11 culturable species from the conventional trout microbiota conferred resistance to F. columnare infection. Using mono-re-conventionalized germ-free trout, we identified that this protection is determined by a commensal Flavobacterium strain displaying antibacterial activity against F. columnare. Finally, we demonstrated that use of gnotobiotic trout is a suitable approach for the identification of both endogenous and exogenous probiotic bacterial strains protecting teleostean hosts against F. columnare. This study therefore establishes an ecologically-relevant gnotobiotic model for the study of host-pathogen interactions and colonization resistance in farmed fish.
url https://doi.org/10.1371/journal.ppat.1009302
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