Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in Vivo

Giardia duodenalis (syn. G. lamblia, G. intestinalis) is the protozoan parasite responsible for giardiasis, the most common and widely spread intestinal parasitic disease worldwide, affecting both humans and animals. After cysts ingestion (through either contaminated food or water), Giardia excysts...

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Main Authors: Thibault Allain, Soraya Chaouch, Myriam Thomas, Isabelle Vallée, André G. Buret, Philippe Langella, Philippe Grellier, Bruno Polack, Luis G. Bermúdez-Humarán, Isabelle Florent
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-01-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.02707/full
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author Thibault Allain
Thibault Allain
Soraya Chaouch
Myriam Thomas
Isabelle Vallée
André G. Buret
Philippe Langella
Philippe Grellier
Bruno Polack
Luis G. Bermúdez-Humarán
Isabelle Florent
author_facet Thibault Allain
Thibault Allain
Soraya Chaouch
Myriam Thomas
Isabelle Vallée
André G. Buret
Philippe Langella
Philippe Grellier
Bruno Polack
Luis G. Bermúdez-Humarán
Isabelle Florent
author_sort Thibault Allain
collection DOAJ
description Giardia duodenalis (syn. G. lamblia, G. intestinalis) is the protozoan parasite responsible for giardiasis, the most common and widely spread intestinal parasitic disease worldwide, affecting both humans and animals. After cysts ingestion (through either contaminated food or water), Giardia excysts in the upper intestinal tract to release replicating trophozoites that are responsible for the production of symptoms. In the gut, Giardia cohabits with the host's microbiota, and several studies have revealed the importance of this gut ecosystem and/or some probiotic bacteria in providing protection against G. duodenalis infection through mechanisms that remain incompletely understood. Recent findings suggest that Bile-Salt-Hydrolase (BSH)-like activities from the probiotic strain of Lactobacillus johnsonii La1 may contribute to the anti-giardial activity displayed by this strain. Here, we cloned and expressed each of the three bsh genes present in the L. johnsonii La1 genome to study their enzymatic and biological properties. While BSH47 and BSH56 were expressed as recombinant active enzymes, no significant enzymatic activity was detected with BSH12. In vitro assays allowed determining the substrate specificities of both BSH47 and BSH56, which were different. Modeling of these BSHs indicated a strong conservation of their 3-D structures despite low conservation of their primary structures. Both recombinant enzymes were able to mediate anti-giardial biological activity against Giardia trophozoites in vitro. Moreover, BSH47 exerted significant anti-giardial effects when tested in a murine model of giardiasis. These results shed new light on the mechanism, whereby active BSH derived from the probiotic strain Lactobacillus johnsonii La1 may yield anti-giardial effects in vitro and in vivo. These findings pave the way toward novel approaches for the treatment of this widely spread but neglected infectious disease, both in human and in veterinary medicine.
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spelling doaj.art-f5cb7f8ad1154b70a6a3d870a16ecd492022-12-22T03:24:28ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-01-01810.3389/fmicb.2017.02707314464Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in VivoThibault Allain0Thibault Allain1Soraya Chaouch2Myriam Thomas3Isabelle Vallée4André G. Buret5Philippe Langella6Philippe Grellier7Bruno Polack8Luis G. Bermúdez-Humarán9Isabelle Florent10Commensal and Probiotics-Host Interactions Laboratory, Micalis Institute, Institut National de la Recherche Agronomique, AgroParisTech, Jouy-en-Josas, FranceUMR7245, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne-Universités, Paris, FranceUMR7245, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne-Universités, Paris, FranceJRU BIPAR, ANSES, Ecole Nationale Vétérinaire d'Alfort, INRA, Université Paris-Est, Animal Health Laboratory, Maisons-Alfort, FranceJRU BIPAR, ANSES, Ecole Nationale Vétérinaire d'Alfort, INRA, Université Paris-Est, Animal Health Laboratory, Maisons-Alfort, FranceDepartment of Biological Sciences, University of Calgary, Calgary, AB, CanadaCommensal and Probiotics-Host Interactions Laboratory, Micalis Institute, Institut National de la Recherche Agronomique, AgroParisTech, Jouy-en-Josas, FranceUMR7245, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne-Universités, Paris, FranceJRU BIPAR, Ecole Nationale Vétérinaire d'Alfort, ANSES, INRA, Université Paris-Est, Maisons-Alfort, FranceCommensal and Probiotics-Host Interactions Laboratory, Micalis Institute, Institut National de la Recherche Agronomique, AgroParisTech, Jouy-en-Josas, FranceUMR7245, Muséum National d'Histoire Naturelle, Centre National de la Recherche Scientifique, Sorbonne-Universités, Paris, FranceGiardia duodenalis (syn. G. lamblia, G. intestinalis) is the protozoan parasite responsible for giardiasis, the most common and widely spread intestinal parasitic disease worldwide, affecting both humans and animals. After cysts ingestion (through either contaminated food or water), Giardia excysts in the upper intestinal tract to release replicating trophozoites that are responsible for the production of symptoms. In the gut, Giardia cohabits with the host's microbiota, and several studies have revealed the importance of this gut ecosystem and/or some probiotic bacteria in providing protection against G. duodenalis infection through mechanisms that remain incompletely understood. Recent findings suggest that Bile-Salt-Hydrolase (BSH)-like activities from the probiotic strain of Lactobacillus johnsonii La1 may contribute to the anti-giardial activity displayed by this strain. Here, we cloned and expressed each of the three bsh genes present in the L. johnsonii La1 genome to study their enzymatic and biological properties. While BSH47 and BSH56 were expressed as recombinant active enzymes, no significant enzymatic activity was detected with BSH12. In vitro assays allowed determining the substrate specificities of both BSH47 and BSH56, which were different. Modeling of these BSHs indicated a strong conservation of their 3-D structures despite low conservation of their primary structures. Both recombinant enzymes were able to mediate anti-giardial biological activity against Giardia trophozoites in vitro. Moreover, BSH47 exerted significant anti-giardial effects when tested in a murine model of giardiasis. These results shed new light on the mechanism, whereby active BSH derived from the probiotic strain Lactobacillus johnsonii La1 may yield anti-giardial effects in vitro and in vivo. These findings pave the way toward novel approaches for the treatment of this widely spread but neglected infectious disease, both in human and in veterinary medicine.http://journal.frontiersin.org/article/10.3389/fmicb.2017.02707/fullGiardia duodenalislactobacilliLactobacillus johnsoniibile salt hydrolasesBSHconjugated bile salts
spellingShingle Thibault Allain
Thibault Allain
Soraya Chaouch
Myriam Thomas
Isabelle Vallée
André G. Buret
Philippe Langella
Philippe Grellier
Bruno Polack
Luis G. Bermúdez-Humarán
Isabelle Florent
Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in Vivo
Frontiers in Microbiology
Giardia duodenalis
lactobacilli
Lactobacillus johnsonii
bile salt hydrolases
BSH
conjugated bile salts
title Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in Vivo
title_full Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in Vivo
title_fullStr Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in Vivo
title_full_unstemmed Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in Vivo
title_short Bile-Salt-Hydrolases from the Probiotic Strain Lactobacillus johnsonii La1 Mediate Anti-giardial Activity in Vitro and in Vivo
title_sort bile salt hydrolases from the probiotic strain lactobacillus johnsonii la1 mediate anti giardial activity in vitro and in vivo
topic Giardia duodenalis
lactobacilli
Lactobacillus johnsonii
bile salt hydrolases
BSH
conjugated bile salts
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.02707/full
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