Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach

The nutritive role and ecology of gut-dwelling microbes in rainbow trout remain enigmatic. To improve our understanding of the rainbow trout gastrointestinal tract (GIT) microbiome, we performed whole shotgun metagenomic analyses on the assembled contigs from luminal contents from both mid- and hind...

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Main Authors: Omolola C. Betiku, Carl J. Yeoman, T. Gibson Gaylord, Suzanne L. Ishaq, Glenn C. Duff, Wendy M. Sealey
Format: Article
Language:English
Published: Elsevier 2023-06-01
Series:Aquaculture Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352513423001400
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author Omolola C. Betiku
Carl J. Yeoman
T. Gibson Gaylord
Suzanne L. Ishaq
Glenn C. Duff
Wendy M. Sealey
author_facet Omolola C. Betiku
Carl J. Yeoman
T. Gibson Gaylord
Suzanne L. Ishaq
Glenn C. Duff
Wendy M. Sealey
author_sort Omolola C. Betiku
collection DOAJ
description The nutritive role and ecology of gut-dwelling microbes in rainbow trout remain enigmatic. To improve our understanding of the rainbow trout gastrointestinal tract (GIT) microbiome, we performed whole shotgun metagenomic analyses on the assembled contigs from luminal contents from both mid- and hind-GIT regions for taxonomic and functional classifications of fish-fed animal and plant protein dietary sources. Our study revealed that trout respond well to the two diets containing animal and plant protein sources when supplemented with essential amino acids to meet the requirements of the fish. Microbes present were predominantly bacteria (89.9%) and mainly of the phyla Tenericutes, Firmicutes, Fusobacteria, and Proteobacteria. Eukaryotic (8.8%) microbes were mainly from phyla Ascomycota and Basidiomycota, while Archaea (<1%) were also present and predominantly from the phylum Euryarchaeota. Comparisons of genus-level classifications and functional profiles revealed compositional differences in these GIT locations that appear modulated by differences in the dietary treatments. The functional analysis provided evidence of amino acid biosynthesis/catabolism and methane production in the mid-GIT, while in the hind-GIT, proteolytic hydrolysis and butyrate metabolism were expressed in the trout fed with plant protein diet. The animal protein-based diet provided metabolites for microbial protein fermentation in the hind-GIT. Our report highlights and identifies the potential nutritive contributions of GIT microbes to trout and a potentially crucial functional division along the GIT. Finally, the plant-based diet enhanced amino acid catabolism in the midgut section, while the hindgut section supports evidence of methanogen fermentation.
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spelling doaj.art-f5e1d252bb9b4bcfa9adda2aa72cb4be2023-06-18T05:02:30ZengElsevierAquaculture Reports2352-51342023-06-0130101601Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approachOmolola C. Betiku0Carl J. Yeoman1T. Gibson Gaylord2Suzanne L. Ishaq3Glenn C. Duff4Wendy M. Sealey5United States Fish and Wildlife Service, Bozeman Fish Technology Center, Bozeman, MT 59715, USA; Department of Animal and Range Science, Montana State University, Bozeman, MT 59717, USA; College of Agriculture and Food Sciences, Florida A&M University, Tallahassee, FL 32307, USA; Corresponding author at: College of Agriculture and Food Sciences, Florida A&M University, Tallahassee, FL 32307, USA.Department of Animal and Range Science, Montana State University, Bozeman, MT 59717, USAUnited States Fish and Wildlife Service, Bozeman Fish Technology Center, Bozeman, MT 59715, USASchool of Food and Agriculture, University of Maine, Orono, ME, USADepartment of Animal and Range Sciences, New Mexico State University, Las Cruces, NM 88003–8003, USAUnited States Fish and Wildlife Service, Bozeman Fish Technology Center, Bozeman, MT 59715, USAThe nutritive role and ecology of gut-dwelling microbes in rainbow trout remain enigmatic. To improve our understanding of the rainbow trout gastrointestinal tract (GIT) microbiome, we performed whole shotgun metagenomic analyses on the assembled contigs from luminal contents from both mid- and hind-GIT regions for taxonomic and functional classifications of fish-fed animal and plant protein dietary sources. Our study revealed that trout respond well to the two diets containing animal and plant protein sources when supplemented with essential amino acids to meet the requirements of the fish. Microbes present were predominantly bacteria (89.9%) and mainly of the phyla Tenericutes, Firmicutes, Fusobacteria, and Proteobacteria. Eukaryotic (8.8%) microbes were mainly from phyla Ascomycota and Basidiomycota, while Archaea (<1%) were also present and predominantly from the phylum Euryarchaeota. Comparisons of genus-level classifications and functional profiles revealed compositional differences in these GIT locations that appear modulated by differences in the dietary treatments. The functional analysis provided evidence of amino acid biosynthesis/catabolism and methane production in the mid-GIT, while in the hind-GIT, proteolytic hydrolysis and butyrate metabolism were expressed in the trout fed with plant protein diet. The animal protein-based diet provided metabolites for microbial protein fermentation in the hind-GIT. Our report highlights and identifies the potential nutritive contributions of GIT microbes to trout and a potentially crucial functional division along the GIT. Finally, the plant-based diet enhanced amino acid catabolism in the midgut section, while the hindgut section supports evidence of methanogen fermentation.http://www.sciencedirect.com/science/article/pii/S2352513423001400Rainbow troutGut microbiomeShotgunMetagenomicsAquacultureNutrition
spellingShingle Omolola C. Betiku
Carl J. Yeoman
T. Gibson Gaylord
Suzanne L. Ishaq
Glenn C. Duff
Wendy M. Sealey
Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach
Aquaculture Reports
Rainbow trout
Gut microbiome
Shotgun
Metagenomics
Aquaculture
Nutrition
title Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach
title_full Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach
title_fullStr Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach
title_full_unstemmed Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach
title_short Evidence of a divided nutritive function in rainbow Trout (Oncorhynchus mykiss) midgut and hindgut microbiomes by whole shotgun metagenomic approach
title_sort evidence of a divided nutritive function in rainbow trout oncorhynchus mykiss midgut and hindgut microbiomes by whole shotgun metagenomic approach
topic Rainbow trout
Gut microbiome
Shotgun
Metagenomics
Aquaculture
Nutrition
url http://www.sciencedirect.com/science/article/pii/S2352513423001400
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