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Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance

Understanding the correlation between shrimp growth and their intestinal bacteria would be necessary to optimize animal’s growth performance. Here, we compared the bacterial profiles along with the shrimp’s gene expression responses and metabolites in the intestines between the Top and the Bottom we...

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Autores principales: Uengwetwanit, Tanaporn, Uawisetwathana, Umaporn, Arayamethakorn, Sopacha, Khudet, Juthatip, Chaiyapechara, Sage, Karoonuthaisiri, Nitsara, Rungrassamee, Wanilada
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7430268/
https://www.ncbi.nlm.nih.gov/pubmed/32864208
http://dx.doi.org/10.7717/peerj.9646
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author Uengwetwanit, Tanaporn
Uawisetwathana, Umaporn
Arayamethakorn, Sopacha
Khudet, Juthatip
Chaiyapechara, Sage
Karoonuthaisiri, Nitsara
Rungrassamee, Wanilada
author_facet Uengwetwanit, Tanaporn
Uawisetwathana, Umaporn
Arayamethakorn, Sopacha
Khudet, Juthatip
Chaiyapechara, Sage
Karoonuthaisiri, Nitsara
Rungrassamee, Wanilada
author_sort Uengwetwanit, Tanaporn
collection PubMed
description Understanding the correlation between shrimp growth and their intestinal bacteria would be necessary to optimize animal’s growth performance. Here, we compared the bacterial profiles along with the shrimp’s gene expression responses and metabolites in the intestines between the Top and the Bottom weight groups. Black tiger shrimp (Penaeus monodon) were collected from the same population and rearing environments. The two weight groups, the Top-weight group with an average weight of 36.82 ± 0.41 g and the Bottom-weight group with an average weight of 17.80 ± 11.81 g, were selected. Intestines were aseptically collected and subjected to microbiota, transcriptomic and metabolomic profile analyses. The weighted-principal coordinates analysis (PCoA) based on UniFrac distances showed similar bacterial profiles between the two groups, suggesting similar relative composition of the overall bacterial community structures. This observed similarity was likely due to the fact that shrimp were from the same genetic background and reared under the same habitat and diets. On the other hand, the unweighted-distance matrix revealed that the bacterial profiles associated in intestines of the Top-weight group were clustered distinctly from those of the Bottom-weight shrimp, suggesting that some unique non-dominant bacterial genera were found associated with either group. The key bacterial members associated to the Top-weight shrimp were mostly from Firmicutes (Brevibacillus and Fusibacter) and Bacteroidetes (Spongiimonas), both of which were found in significantly higher abundance than those of the Bottom-weight shrimp. Transcriptomic profile of shrimp intestines found significant upregulation of genes mostly involved in nutrient metabolisms and energy storage in the Top-weight shrimp. In addition to significantly expressed metabolic-related genes, the Bottom-weight shrimp also showed significant upregulation of stress and immune-related genes, suggesting that these pathways might contribute to different degrees of shrimp growth performance. A non-targeted metabolome analysis from shrimp intestines revealed different metabolic responsive patterns, in which the Top-weight shrimp contained significantly higher levels of short chain fatty acids, lipids and organic compounds than the Bottom-weight shrimp. The identified metabolites included those that were known to be produced by intestinal bacteria such as butyric acid, 4-indolecarbaldehyde and L-3-phenyllactic acid as well as those produced by shrimp such as acyl-carnitines and lysophosphatidylcholine. The functions of these metabolites were related to nutrient absorption and metabolisms. Our findings provide the first report utilizing multi-omics integration approach to investigate microbiota, metabolic and transcriptomics profiles of the host shrimp and their potential roles and relationship to shrimp growth performance.
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spelling pubmed-74302682020-08-27 Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance Uengwetwanit, Tanaporn Uawisetwathana, Umaporn Arayamethakorn, Sopacha Khudet, Juthatip Chaiyapechara, Sage Karoonuthaisiri, Nitsara Rungrassamee, Wanilada PeerJ Aquaculture, Fisheries and Fish Science Understanding the correlation between shrimp growth and their intestinal bacteria would be necessary to optimize animal’s growth performance. Here, we compared the bacterial profiles along with the shrimp’s gene expression responses and metabolites in the intestines between the Top and the Bottom weight groups. Black tiger shrimp (Penaeus monodon) were collected from the same population and rearing environments. The two weight groups, the Top-weight group with an average weight of 36.82 ± 0.41 g and the Bottom-weight group with an average weight of 17.80 ± 11.81 g, were selected. Intestines were aseptically collected and subjected to microbiota, transcriptomic and metabolomic profile analyses. The weighted-principal coordinates analysis (PCoA) based on UniFrac distances showed similar bacterial profiles between the two groups, suggesting similar relative composition of the overall bacterial community structures. This observed similarity was likely due to the fact that shrimp were from the same genetic background and reared under the same habitat and diets. On the other hand, the unweighted-distance matrix revealed that the bacterial profiles associated in intestines of the Top-weight group were clustered distinctly from those of the Bottom-weight shrimp, suggesting that some unique non-dominant bacterial genera were found associated with either group. The key bacterial members associated to the Top-weight shrimp were mostly from Firmicutes (Brevibacillus and Fusibacter) and Bacteroidetes (Spongiimonas), both of which were found in significantly higher abundance than those of the Bottom-weight shrimp. Transcriptomic profile of shrimp intestines found significant upregulation of genes mostly involved in nutrient metabolisms and energy storage in the Top-weight shrimp. In addition to significantly expressed metabolic-related genes, the Bottom-weight shrimp also showed significant upregulation of stress and immune-related genes, suggesting that these pathways might contribute to different degrees of shrimp growth performance. A non-targeted metabolome analysis from shrimp intestines revealed different metabolic responsive patterns, in which the Top-weight shrimp contained significantly higher levels of short chain fatty acids, lipids and organic compounds than the Bottom-weight shrimp. The identified metabolites included those that were known to be produced by intestinal bacteria such as butyric acid, 4-indolecarbaldehyde and L-3-phenyllactic acid as well as those produced by shrimp such as acyl-carnitines and lysophosphatidylcholine. The functions of these metabolites were related to nutrient absorption and metabolisms. Our findings provide the first report utilizing multi-omics integration approach to investigate microbiota, metabolic and transcriptomics profiles of the host shrimp and their potential roles and relationship to shrimp growth performance. PeerJ Inc. 2020-08-14 /pmc/articles/PMC7430268/ /pubmed/32864208 http://dx.doi.org/10.7717/peerj.9646 Text en ©2020 Uengwetwanit et al. https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Aquaculture, Fisheries and Fish Science
Uengwetwanit, Tanaporn
Uawisetwathana, Umaporn
Arayamethakorn, Sopacha
Khudet, Juthatip
Chaiyapechara, Sage
Karoonuthaisiri, Nitsara
Rungrassamee, Wanilada
Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance
title Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance
title_full Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance
title_fullStr Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance
title_full_unstemmed Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance
title_short Multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (Penaeus monodon) with different growth performance
title_sort multi-omics analysis to examine microbiota, host gene expression and metabolites in the intestine of black tiger shrimp (penaeus monodon) with different growth performance
topic Aquaculture, Fisheries and Fish Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7430268/
https://www.ncbi.nlm.nih.gov/pubmed/32864208
http://dx.doi.org/10.7717/peerj.9646
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