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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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 |
work_keys_str_mv |
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