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The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp

SIMPLE SUMMARY: The harsh aquatic environment makes the use of dietary probiotics not cost-effective and with low efficacy due to their inability to reach the gut. Therefore, supporting the growth of commensal probiotic bacteria, in aquatic animals, represents an efficient strategy to improve and ma...

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Autores principales: Butucel, Eugenia, Balta, Igori, McCleery, David, Marcu, Adela, Stef, Ducu, Pet, Ioan, Callaway, Todd, Stef, Lavinia, Corcionivoschi, Nicolae
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9855566/
https://www.ncbi.nlm.nih.gov/pubmed/36671749
http://dx.doi.org/10.3390/biology12010057
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author Butucel, Eugenia
Balta, Igori
McCleery, David
Marcu, Adela
Stef, Ducu
Pet, Ioan
Callaway, Todd
Stef, Lavinia
Corcionivoschi, Nicolae
author_facet Butucel, Eugenia
Balta, Igori
McCleery, David
Marcu, Adela
Stef, Ducu
Pet, Ioan
Callaway, Todd
Stef, Lavinia
Corcionivoschi, Nicolae
author_sort Butucel, Eugenia
collection PubMed
description SIMPLE SUMMARY: The harsh aquatic environment makes the use of dietary probiotics not cost-effective and with low efficacy due to their inability to reach the gut. Therefore, supporting the growth of commensal probiotic bacteria, in aquatic animals, represents an efficient strategy to improve and maintain their gut health. The commensal probiotic, Faecalibacterium prausnitzii, is well known for its association with improved gut health in humans, farm animals and crustaceans. As such, increasing its abundance in the gut is of major interest and, moreover, identification of interventions able to support its growth is necessary. Undoubtedly, organic compounds, such as mixtures of organic acids, have a role in improving gut health and supporting the gut microbiota in either fighting disease or improving digestion. With this study, we aimed to further understand the biological mechanisms by which F. prausnitzii inhibits pathogenic bacteria, in the presence of organic acids. Furthermore, we have also investigated the organic acid ability to stimulate bacterial growth in vitro and ex vivo. Herein we show that a mixture of organic acids, AuraAqua (Aq) leads to improved F. prausnitzii growth and butyrate production which consequently reduces V. parahaemolyticus infection of shrimp gut primary epithelial cells. ABSTRACT: Increasing the abundance of probiotic bacteria in the gut requires either direct dietary supplementation or the inclusion of feed additives able to support the growth of beneficial commensal bacteria. In crustaceans, the increased presence of probiotic-like bacteria in the gut, including of Faecalibacterium prausnitzii (F. prausnitzii), will guarantee a positive health status and a gut environment that will ensure enhanced performance. The aim of this study was to investigate if a mixture of organic acids, AuraAqua (Aq) can stimulate the growth and the anti-pathogenic efficacy of F. prausnitzii through a combination of in vitro and ex vivo models. The results showed that 0.5% Aq was able to improve the growth rate of F. prausnitzii in vitro and in an ex vivo shrimp gut model. Moreover, we were able to demonstrate that Aq increases butyrate production and cellulose degradation in culture or in the shrimp gut model. The growth-stimulating effect of Aq also led to an improved and anti-pathogenic effect against Vibrio parahaemolyticus in a co-culture experiment with shrimp gut primary epithelial cells (SGP). In conclusion, our work demonstrates that Aq can stimulate the growth of F. prausnitzii, increase the production of short-chain fatty acid (SCFA) butyrate, improve substrate digestion, and prevent V. parahaemolyticus invasion of SGP cells.
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spelling pubmed-98555662023-01-21 The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp Butucel, Eugenia Balta, Igori McCleery, David Marcu, Adela Stef, Ducu Pet, Ioan Callaway, Todd Stef, Lavinia Corcionivoschi, Nicolae Biology (Basel) Article SIMPLE SUMMARY: The harsh aquatic environment makes the use of dietary probiotics not cost-effective and with low efficacy due to their inability to reach the gut. Therefore, supporting the growth of commensal probiotic bacteria, in aquatic animals, represents an efficient strategy to improve and maintain their gut health. The commensal probiotic, Faecalibacterium prausnitzii, is well known for its association with improved gut health in humans, farm animals and crustaceans. As such, increasing its abundance in the gut is of major interest and, moreover, identification of interventions able to support its growth is necessary. Undoubtedly, organic compounds, such as mixtures of organic acids, have a role in improving gut health and supporting the gut microbiota in either fighting disease or improving digestion. With this study, we aimed to further understand the biological mechanisms by which F. prausnitzii inhibits pathogenic bacteria, in the presence of organic acids. Furthermore, we have also investigated the organic acid ability to stimulate bacterial growth in vitro and ex vivo. Herein we show that a mixture of organic acids, AuraAqua (Aq) leads to improved F. prausnitzii growth and butyrate production which consequently reduces V. parahaemolyticus infection of shrimp gut primary epithelial cells. ABSTRACT: Increasing the abundance of probiotic bacteria in the gut requires either direct dietary supplementation or the inclusion of feed additives able to support the growth of beneficial commensal bacteria. In crustaceans, the increased presence of probiotic-like bacteria in the gut, including of Faecalibacterium prausnitzii (F. prausnitzii), will guarantee a positive health status and a gut environment that will ensure enhanced performance. The aim of this study was to investigate if a mixture of organic acids, AuraAqua (Aq) can stimulate the growth and the anti-pathogenic efficacy of F. prausnitzii through a combination of in vitro and ex vivo models. The results showed that 0.5% Aq was able to improve the growth rate of F. prausnitzii in vitro and in an ex vivo shrimp gut model. Moreover, we were able to demonstrate that Aq increases butyrate production and cellulose degradation in culture or in the shrimp gut model. The growth-stimulating effect of Aq also led to an improved and anti-pathogenic effect against Vibrio parahaemolyticus in a co-culture experiment with shrimp gut primary epithelial cells (SGP). In conclusion, our work demonstrates that Aq can stimulate the growth of F. prausnitzii, increase the production of short-chain fatty acid (SCFA) butyrate, improve substrate digestion, and prevent V. parahaemolyticus invasion of SGP cells. MDPI 2022-12-29 /pmc/articles/PMC9855566/ /pubmed/36671749 http://dx.doi.org/10.3390/biology12010057 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Butucel, Eugenia
Balta, Igori
McCleery, David
Marcu, Adela
Stef, Ducu
Pet, Ioan
Callaway, Todd
Stef, Lavinia
Corcionivoschi, Nicolae
The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp
title The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp
title_full The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp
title_fullStr The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp
title_full_unstemmed The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp
title_short The Prebiotic Effect of an Organic Acid Mixture on Faecalibacterium prausnitzii Metabolism and Its Anti-Pathogenic Role against Vibrio parahaemolyticus in Shrimp
title_sort prebiotic effect of an organic acid mixture on faecalibacterium prausnitzii metabolism and its anti-pathogenic role against vibrio parahaemolyticus in shrimp
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9855566/
https://www.ncbi.nlm.nih.gov/pubmed/36671749
http://dx.doi.org/10.3390/biology12010057
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