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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Main Authors: Ryan C. McDonald, Joy E. M. Watts, Harold J. Schreier
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-11-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fmicb.2019.02687/full
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spelling doaj-8987fd8a41da4ee782e6cb42270375a02020-11-25T02:51:46ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2019-11-011010.3389/fmicb.2019.02687491631Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatusRyan C. McDonald0Joy E. M. Watts1Harold J. Schreier2Harold J. Schreier3Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, MD, United StatesDepartment of Biological Sciences, University of Portsmouth, Portsmouth, United KingdomDepartment of Biological Sciences, University of Maryland, Baltimore County, Baltimore, MD, United StatesDepartment of Marine Biotechnology, University of Maryland, Baltimore County, Baltimore, MD, United StatesWood 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.https://www.frontiersin.org/article/10.3389/fmicb.2019.02687/fulllignocellulose digestionmicrobiome16S rRNA gene amplicon sequencingpredictive metagenomicsAmazonian catfish
collection DOAJ
language English
format Article
sources DOAJ
author Ryan C. McDonald
Joy E. M. Watts
Harold J. Schreier
Harold J. Schreier
spellingShingle Ryan C. McDonald
Joy E. M. Watts
Harold J. Schreier
Harold J. Schreier
Effect of Diet on the Enteric Microbiome of the Wood-Eating Catfish Panaque nigrolineatus
Frontiers in Microbiology
lignocellulose digestion
microbiome
16S rRNA gene amplicon sequencing
predictive metagenomics
Amazonian catfish
author_facet Ryan C. McDonald
Joy E. M. Watts
Harold J. Schreier
Harold J. Schreier
author_sort Ryan C. McDonald
title 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_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_sort effect of diet on the enteric microbiome of the wood-eating catfish panaque nigrolineatus
publisher Frontiers Media S.A.
series Frontiers in Microbiology
issn 1664-302X
publishDate 2019-11-01
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.
topic lignocellulose digestion
microbiome
16S rRNA gene amplicon sequencing
predictive metagenomics
Amazonian catfish
url https://www.frontiersin.org/article/10.3389/fmicb.2019.02687/full
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