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Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals

The aquaculture industry is one of the fastest-growing sectors in animal food production. However, farming of carnivorous fish strongly relies on the use of wild fish-based meals, a practice that is environmentally and economically unsustainable. Insect-based diets constitute a strong candidate for...

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Autores principales: Rangel, Fábio, Enes, Paula, Gasco, Laura, Gai, Francesco, Hausmann, Bela, Berry, David, Oliva-Teles, Aires, Serra, Claudia R., Pereira, Fátima C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9041418/
https://www.ncbi.nlm.nih.gov/pubmed/35495644
http://dx.doi.org/10.3389/fmicb.2022.831034
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author Rangel, Fábio
Enes, Paula
Gasco, Laura
Gai, Francesco
Hausmann, Bela
Berry, David
Oliva-Teles, Aires
Serra, Claudia R.
Pereira, Fátima C.
author_facet Rangel, Fábio
Enes, Paula
Gasco, Laura
Gai, Francesco
Hausmann, Bela
Berry, David
Oliva-Teles, Aires
Serra, Claudia R.
Pereira, Fátima C.
author_sort Rangel, Fábio
collection PubMed
description The aquaculture industry is one of the fastest-growing sectors in animal food production. However, farming of carnivorous fish strongly relies on the use of wild fish-based meals, a practice that is environmentally and economically unsustainable. Insect-based diets constitute a strong candidate for fishmeal substitution, due to their high nutritional value and low environmental footprint. Nevertheless, data on the impact of insect meal (IM) on the gut microbiome of farmed fish are so far inconclusive, and very scarce in what concerns modulation of microbial-mediated functions. Here we use high-throughput 16S rRNA gene amplicon sequencing and quantitative PCR to evaluate the impact of different IMs on the composition and chitinolytic potential of the European sea bass gut digesta- and mucosa-associated communities. Our results show that insect-based diets of distinct origins differently impact the gut microbiota of the European sea bass (Dicentrarchus labrax). We detected clear modulatory effects of IM on the gut microbiota, which were more pronounced in the digesta, where communities differed considerably among the diets tested. Major community shifts were associated with the use of black soldier fly larvae (Hermetia illucens, HM) and pupal exuviae (HEM) feeds and were characterized by an increase in the relative abundance of the Firmicutes families Bacillaceae, Enterococcaceae, and Lachnospiraceae and the Actinobacteria family Actinomycetaceae, which all include taxa considered beneficial for fish health. Modulation of the digesta community by HEM was characterized by a sharp increase in Paenibacillus and a decrease of several Gammaproteobacteria and Bacteroidota members. In turn, a mealworm larvae-based diet (Tenebrio molitor, TM) had only a modest impact on microbiota composition. Further, using quantitative PCR, we demonstrate that shifts induced by HEM were accompanied by an increase in copy number of chitinase ChiA-encoding genes, predominantly originating from Paenibacillus species with effective chitinolytic activity. Our study reveals an HEM-driven increase in chitin-degrading taxa and associated chitinolytic activity, uncovering potential benefits of adopting exuviae-supplemented diets, a waste product of insect rearing, as a functional ingredient.
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spelling pubmed-90414182022-04-27 Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals Rangel, Fábio Enes, Paula Gasco, Laura Gai, Francesco Hausmann, Bela Berry, David Oliva-Teles, Aires Serra, Claudia R. Pereira, Fátima C. Front Microbiol Microbiology The aquaculture industry is one of the fastest-growing sectors in animal food production. However, farming of carnivorous fish strongly relies on the use of wild fish-based meals, a practice that is environmentally and economically unsustainable. Insect-based diets constitute a strong candidate for fishmeal substitution, due to their high nutritional value and low environmental footprint. Nevertheless, data on the impact of insect meal (IM) on the gut microbiome of farmed fish are so far inconclusive, and very scarce in what concerns modulation of microbial-mediated functions. Here we use high-throughput 16S rRNA gene amplicon sequencing and quantitative PCR to evaluate the impact of different IMs on the composition and chitinolytic potential of the European sea bass gut digesta- and mucosa-associated communities. Our results show that insect-based diets of distinct origins differently impact the gut microbiota of the European sea bass (Dicentrarchus labrax). We detected clear modulatory effects of IM on the gut microbiota, which were more pronounced in the digesta, where communities differed considerably among the diets tested. Major community shifts were associated with the use of black soldier fly larvae (Hermetia illucens, HM) and pupal exuviae (HEM) feeds and were characterized by an increase in the relative abundance of the Firmicutes families Bacillaceae, Enterococcaceae, and Lachnospiraceae and the Actinobacteria family Actinomycetaceae, which all include taxa considered beneficial for fish health. Modulation of the digesta community by HEM was characterized by a sharp increase in Paenibacillus and a decrease of several Gammaproteobacteria and Bacteroidota members. In turn, a mealworm larvae-based diet (Tenebrio molitor, TM) had only a modest impact on microbiota composition. Further, using quantitative PCR, we demonstrate that shifts induced by HEM were accompanied by an increase in copy number of chitinase ChiA-encoding genes, predominantly originating from Paenibacillus species with effective chitinolytic activity. Our study reveals an HEM-driven increase in chitin-degrading taxa and associated chitinolytic activity, uncovering potential benefits of adopting exuviae-supplemented diets, a waste product of insect rearing, as a functional ingredient. Frontiers Media S.A. 2022-04-12 /pmc/articles/PMC9041418/ /pubmed/35495644 http://dx.doi.org/10.3389/fmicb.2022.831034 Text en Copyright © 2022 Rangel, Enes, Gasco, Gai, Hausmann, Berry, Oliva-Teles, Serra and Pereira. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Rangel, Fábio
Enes, Paula
Gasco, Laura
Gai, Francesco
Hausmann, Bela
Berry, David
Oliva-Teles, Aires
Serra, Claudia R.
Pereira, Fátima C.
Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals
title Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals
title_full Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals
title_fullStr Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals
title_full_unstemmed Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals
title_short Differential Modulation of the European Sea Bass Gut Microbiota by Distinct Insect Meals
title_sort differential modulation of the european sea bass gut microbiota by distinct insect meals
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9041418/
https://www.ncbi.nlm.nih.gov/pubmed/35495644
http://dx.doi.org/10.3389/fmicb.2022.831034
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