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Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection

Omega-3 polyunsaturated fatty acids (n-3 PUFAs), such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), exhibit antibacterial and anti-inflammatory activities. Furthermore, diets rich in n-3 PUFAs are known to improve disease resistance and limit pathogen infection in commercial aquacul...

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Autores principales: Chiang, Keng-Yu, Lin, Wen-Chun, Tsai, Tsung-Yu, Lin, Cheng-Wei, Huang, Shin-Jie, Huang, Ching-Yu, Wu, Sheng-Han, Ken, Chuian-Fu, Gong, Hong-Yi, Chen, Jyh-Yih, Wu, Jen-Leih
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7392239/
https://www.ncbi.nlm.nih.gov/pubmed/32730353
http://dx.doi.org/10.1371/journal.pone.0236601
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author Chiang, Keng-Yu
Lin, Wen-Chun
Tsai, Tsung-Yu
Lin, Cheng-Wei
Huang, Shin-Jie
Huang, Ching-Yu
Wu, Sheng-Han
Ken, Chuian-Fu
Gong, Hong-Yi
Chen, Jyh-Yih
Wu, Jen-Leih
author_facet Chiang, Keng-Yu
Lin, Wen-Chun
Tsai, Tsung-Yu
Lin, Cheng-Wei
Huang, Shin-Jie
Huang, Ching-Yu
Wu, Sheng-Han
Ken, Chuian-Fu
Gong, Hong-Yi
Chen, Jyh-Yih
Wu, Jen-Leih
author_sort Chiang, Keng-Yu
collection PubMed
description Omega-3 polyunsaturated fatty acids (n-3 PUFAs), such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), exhibit antibacterial and anti-inflammatory activities. Furthermore, diets rich in n-3 PUFAs are known to improve disease resistance and limit pathogen infection in commercial aquaculture fishes. In this study, we examined the effects of transgenic overexpression of n-3 PUFA biosynthesis genes on the physiological response to bacterial infection in tilapia. We first established tilapia strains with single or dual expression of salmon delta-5 desaturase and/or delta-6 desaturase and then challenged the fish with Vibrio vulnificus infection. Interestingly, our data suggest that n-3 PUFA-mediated alterations in gut microbiota may be important in determining disease outcome via effects on immune response of the host. Both liver- and muscle-specific single and dual expression of delta-5 desaturase and delta-6 desaturase resulted in higher n-3 PUFA content in transgenic fish fed with a LO basal diet. The enrichment of n-3 PUFAs in dual-transgenic fish is likely responsible for their improved survival rate and comparatively reduced expression of inflammation- and immune-associated genes after V. vulnificus infection. Gut microbiome analysis further revealed that dual-transgenic tilapia had high gut microbiota diversity, with low levels of inflammation-associated microbiota (i.e., Prevotellaceae). Thus, our findings indicate that dual expression of transgenic delta-5 and delta-6 desaturase in tilapia enhances disease resistance, an effect that is associated with increased levels of n-3 PUFAs and altered gut microbiota composition.
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spelling pubmed-73922392020-08-05 Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection Chiang, Keng-Yu Lin, Wen-Chun Tsai, Tsung-Yu Lin, Cheng-Wei Huang, Shin-Jie Huang, Ching-Yu Wu, Sheng-Han Ken, Chuian-Fu Gong, Hong-Yi Chen, Jyh-Yih Wu, Jen-Leih PLoS One Research Article Omega-3 polyunsaturated fatty acids (n-3 PUFAs), such as eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), exhibit antibacterial and anti-inflammatory activities. Furthermore, diets rich in n-3 PUFAs are known to improve disease resistance and limit pathogen infection in commercial aquaculture fishes. In this study, we examined the effects of transgenic overexpression of n-3 PUFA biosynthesis genes on the physiological response to bacterial infection in tilapia. We first established tilapia strains with single or dual expression of salmon delta-5 desaturase and/or delta-6 desaturase and then challenged the fish with Vibrio vulnificus infection. Interestingly, our data suggest that n-3 PUFA-mediated alterations in gut microbiota may be important in determining disease outcome via effects on immune response of the host. Both liver- and muscle-specific single and dual expression of delta-5 desaturase and delta-6 desaturase resulted in higher n-3 PUFA content in transgenic fish fed with a LO basal diet. The enrichment of n-3 PUFAs in dual-transgenic fish is likely responsible for their improved survival rate and comparatively reduced expression of inflammation- and immune-associated genes after V. vulnificus infection. Gut microbiome analysis further revealed that dual-transgenic tilapia had high gut microbiota diversity, with low levels of inflammation-associated microbiota (i.e., Prevotellaceae). Thus, our findings indicate that dual expression of transgenic delta-5 and delta-6 desaturase in tilapia enhances disease resistance, an effect that is associated with increased levels of n-3 PUFAs and altered gut microbiota composition. Public Library of Science 2020-07-30 /pmc/articles/PMC7392239/ /pubmed/32730353 http://dx.doi.org/10.1371/journal.pone.0236601 Text en © 2020 Chiang et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Chiang, Keng-Yu
Lin, Wen-Chun
Tsai, Tsung-Yu
Lin, Cheng-Wei
Huang, Shin-Jie
Huang, Ching-Yu
Wu, Sheng-Han
Ken, Chuian-Fu
Gong, Hong-Yi
Chen, Jyh-Yih
Wu, Jen-Leih
Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection
title Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection
title_full Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection
title_fullStr Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection
title_full_unstemmed Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection
title_short Dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to Vibrio vulnificus infection
title_sort dual expression of transgenic delta-5 and delta-6 desaturase in tilapia alters gut microbiota and enhances resistance to vibrio vulnificus infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7392239/
https://www.ncbi.nlm.nih.gov/pubmed/32730353
http://dx.doi.org/10.1371/journal.pone.0236601
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