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Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus

Wood is consistently found in high levels in the gastrointestinal tract of the Amazonian catfish Panaque nigrolineatus, which, depending on environmental conditions, can switch between xylivorous and detritivorous dietary strategies. This is highly unusual among primary wood consumers and provides a...

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Autores principales: McDonald, Ryan C., Watts, Joy E. M., Schreier, Harold J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6895002/
https://www.ncbi.nlm.nih.gov/pubmed/31849863
http://dx.doi.org/10.3389/fmicb.2019.02687
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author McDonald, Ryan C.
Watts, Joy E. M.
Schreier, Harold J.
author_facet McDonald, Ryan C.
Watts, Joy E. M.
Schreier, Harold J.
author_sort McDonald, Ryan C.
collection PubMed
description Wood is consistently found in high levels in the gastrointestinal tract of the Amazonian catfish Panaque nigrolineatus, which, depending on environmental conditions, can switch between xylivorous and detritivorous dietary strategies. This is highly unusual among primary wood consumers and provides a unique system to examine the effect of dietary change in a xylivorous system. In this study, microbiome and predictive metagenomic analyses were performed for P. nigrolineatus fed either wood alone or a less refractory mixed diet containing wood and plant nutrition. While diet had an impact on enteric bacterial community composition, there was a high degree of interindividual variability. Members of the Proteobacteria and Planctomycetes were ubiquitous and dominated most communities; Bacteroidetes, Fusobacteria, Actinobacteria, and Verrucomicrobia also contributed in a tissue and diet-specific manner. Although predictive metagenomics revealed functional differences between communities, the relative abundance of predicted lignocellulose-active enzymes remained similar across diets. The microbiomes from both diets appeared highly adapted for hemicellulose hydrolysis as the predicted metagenomes contained several classes of hemicellulases and lignin-modifying enzymes. Enteric communities from both diets appeared to lack the necessary cellobiohydrolases for efficient cellulose hydrolysis, suggesting that cellobiose is not the primary source of dietary carbon for the fish. Our findings suggest that the P. nigrolineatus gut environment selects for an enteric community based on function, rather than a vertically transferred symbiotic relationship. This functional selection strategy may provide an advantage to an organism that switches between dietary strategies to survive a highly variable environment.
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spelling pubmed-68950022019-12-17 Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus McDonald, Ryan C. Watts, Joy E. M. Schreier, Harold J. Front Microbiol Microbiology Wood is consistently found in high levels in the gastrointestinal tract of the Amazonian catfish Panaque nigrolineatus, which, depending on environmental conditions, can switch between xylivorous and detritivorous dietary strategies. This is highly unusual among primary wood consumers and provides a unique system to examine the effect of dietary change in a xylivorous system. In this study, microbiome and predictive metagenomic analyses were performed for P. nigrolineatus fed either wood alone or a less refractory mixed diet containing wood and plant nutrition. While diet had an impact on enteric bacterial community composition, there was a high degree of interindividual variability. Members of the Proteobacteria and Planctomycetes were ubiquitous and dominated most communities; Bacteroidetes, Fusobacteria, Actinobacteria, and Verrucomicrobia also contributed in a tissue and diet-specific manner. Although predictive metagenomics revealed functional differences between communities, the relative abundance of predicted lignocellulose-active enzymes remained similar across diets. The microbiomes from both diets appeared highly adapted for hemicellulose hydrolysis as the predicted metagenomes contained several classes of hemicellulases and lignin-modifying enzymes. Enteric communities from both diets appeared to lack the necessary cellobiohydrolases for efficient cellulose hydrolysis, suggesting that cellobiose is not the primary source of dietary carbon for the fish. Our findings suggest that the P. nigrolineatus gut environment selects for an enteric community based on function, rather than a vertically transferred symbiotic relationship. This functional selection strategy may provide an advantage to an organism that switches between dietary strategies to survive a highly variable environment. Frontiers Media S.A. 2019-11-29 /pmc/articles/PMC6895002/ /pubmed/31849863 http://dx.doi.org/10.3389/fmicb.2019.02687 Text en Copyright © 2019 McDonald, Watts and Schreier. http://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
McDonald, Ryan C.
Watts, Joy E. M.
Schreier, Harold J.
Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus
title Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus
title_full Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus
title_fullStr Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus
title_full_unstemmed Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus
title_short Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus
title_sort effect of diet on the enteric microbiome of the wood-eating catfish panaque nigrolineatus
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6895002/
https://www.ncbi.nlm.nih.gov/pubmed/31849863
http://dx.doi.org/10.3389/fmicb.2019.02687
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