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Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures

Infectious hematopoietic necrosis (IHN) is a major disease that limits the culture of rainbow trout. In practical production, it has been found that the temperature of the culture water is a crucial factor affecting its mortality. Currently, little is known about how temperature affects the immune r...

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Autores principales: Hai, Qiang, Wang, Jianfu, Kang, Weiguo, Cheng, Shuru, Li, Jie, Lyu, Nana, Li, Yajun, Luo, Zhiyuan, Liu, Zhe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10614001/
https://www.ncbi.nlm.nih.gov/pubmed/37908544
http://dx.doi.org/10.3389/fmicb.2023.1275649
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author Hai, Qiang
Wang, Jianfu
Kang, Weiguo
Cheng, Shuru
Li, Jie
Lyu, Nana
Li, Yajun
Luo, Zhiyuan
Liu, Zhe
author_facet Hai, Qiang
Wang, Jianfu
Kang, Weiguo
Cheng, Shuru
Li, Jie
Lyu, Nana
Li, Yajun
Luo, Zhiyuan
Liu, Zhe
author_sort Hai, Qiang
collection PubMed
description Infectious hematopoietic necrosis (IHN) is a major disease that limits the culture of rainbow trout. In practical production, it has been found that the temperature of the culture water is a crucial factor affecting its mortality. Currently, little is known about how temperature affects the immune response of rainbow trout gut microbiota and metabolites to IHNV. In this study, our main objective is to analyze the changes in gut microorganisms of rainbow trout (juvenile fish with a consistent genetic background) after 14 days of infection with IHNV (5 × 10(5) pfu/fish) at 12–13°C (C: injected with saline, A: injected with IHNV) and 16–17°C (D: injected with saline, B: injected with IHNV) using metagenomic and metabolomic analyses, and to screen for probiotics that are effective against IHNV. The results showed that infection with IHNV at 12–13°C caused Eukaryote loss. Compared to Group C, Group A showed a significant increase in harmful pathogens, such as Yersiniaceae, and a significant alteration of 4,087 gut metabolites. Compared to group D, group B showed a significant increase in the abundance of Streptococcaceae and Lactococcus lactis, along with significant changes in 4,259 intestinal metabolites. Compared with their respective groups, the levels of two immune-related metabolites, 1-Octadecanoyl-glycero-3-phosphoethanolamine and L-Glutamate, were significantly upregulated in groups A and B. Compared to group B, Group A showed significantly higher pathogenic bacteria including Aeromonas, Pseudomonas, and Yersiniaceae, while group B showed a significant increase in Streptococcaceae and Lactococcus lactis. Additionally, there were 4,018 significantly different metabolites between the two groups. Interestingly, 1-Octadecanoyl-sn-glycero-3-phosphoethanolamine and L-Glutamate were significantly higher in group A than in group B. Some of the different metabolites in C vs. A are correlated with Fomitopsis pinicola, while in D vs. B they were correlated with Lactococcus raffinolactis, and in A vs. B they were correlated with Hypsizygus marmoreus. This study exposed how rainbow trout gut microbiota and metabolites respond to IHNV at different temperatures, and screens beneficial bacteria with potential resistance to IHN, providing new insights and scientific basis for the prevention and treatment of IHN.
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spelling pubmed-106140012023-10-31 Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures Hai, Qiang Wang, Jianfu Kang, Weiguo Cheng, Shuru Li, Jie Lyu, Nana Li, Yajun Luo, Zhiyuan Liu, Zhe Front Microbiol Microbiology Infectious hematopoietic necrosis (IHN) is a major disease that limits the culture of rainbow trout. In practical production, it has been found that the temperature of the culture water is a crucial factor affecting its mortality. Currently, little is known about how temperature affects the immune response of rainbow trout gut microbiota and metabolites to IHNV. In this study, our main objective is to analyze the changes in gut microorganisms of rainbow trout (juvenile fish with a consistent genetic background) after 14 days of infection with IHNV (5 × 10(5) pfu/fish) at 12–13°C (C: injected with saline, A: injected with IHNV) and 16–17°C (D: injected with saline, B: injected with IHNV) using metagenomic and metabolomic analyses, and to screen for probiotics that are effective against IHNV. The results showed that infection with IHNV at 12–13°C caused Eukaryote loss. Compared to Group C, Group A showed a significant increase in harmful pathogens, such as Yersiniaceae, and a significant alteration of 4,087 gut metabolites. Compared to group D, group B showed a significant increase in the abundance of Streptococcaceae and Lactococcus lactis, along with significant changes in 4,259 intestinal metabolites. Compared with their respective groups, the levels of two immune-related metabolites, 1-Octadecanoyl-glycero-3-phosphoethanolamine and L-Glutamate, were significantly upregulated in groups A and B. Compared to group B, Group A showed significantly higher pathogenic bacteria including Aeromonas, Pseudomonas, and Yersiniaceae, while group B showed a significant increase in Streptococcaceae and Lactococcus lactis. Additionally, there were 4,018 significantly different metabolites between the two groups. Interestingly, 1-Octadecanoyl-sn-glycero-3-phosphoethanolamine and L-Glutamate were significantly higher in group A than in group B. Some of the different metabolites in C vs. A are correlated with Fomitopsis pinicola, while in D vs. B they were correlated with Lactococcus raffinolactis, and in A vs. B they were correlated with Hypsizygus marmoreus. This study exposed how rainbow trout gut microbiota and metabolites respond to IHNV at different temperatures, and screens beneficial bacteria with potential resistance to IHN, providing new insights and scientific basis for the prevention and treatment of IHN. Frontiers Media S.A. 2023-10-16 /pmc/articles/PMC10614001/ /pubmed/37908544 http://dx.doi.org/10.3389/fmicb.2023.1275649 Text en Copyright © 2023 Hai, Wang, Kang, Cheng, Li, Lyu, Li, Luo and Liu. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Hai, Qiang
Wang, Jianfu
Kang, Weiguo
Cheng, Shuru
Li, Jie
Lyu, Nana
Li, Yajun
Luo, Zhiyuan
Liu, Zhe
Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures
title Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures
title_full Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures
title_fullStr Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures
title_full_unstemmed Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures
title_short Metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (Oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures
title_sort metagenomic and metabolomic analysis of changes in intestinal contents of rainbow trout (oncorhynchus mykiss) infected with infectious hematopoietic necrosis virus at different culture water temperatures
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10614001/
https://www.ncbi.nlm.nih.gov/pubmed/37908544
http://dx.doi.org/10.3389/fmicb.2023.1275649
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