Hypoxia stress alters gene expression in the gills and spleen of greater amberjack (Serioladumerili)

Greater amberjack (Seriola dumerili) is a fish species that has significant economic and cultural value. It has a large size and grows rapidly. However, the intolerance to hypoxia poses a major obstacle to the growth of its aquaculture industry. This study focuses on the gills and spleen, two organs...

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Veröffentlicht in:Fish & shellfish immunology 2024-07, Vol.150, p.109602-109602, Article 109602
Hauptverfasser: Li, Duo, Zhang, Weiwei, Wang, Tong, Yang, Yang, Hua, Sijie, Ruan, Qingxin, Wang, Xi, Zhu, Chunhua, Meng, Zining
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container_start_page 109602
container_title Fish & shellfish immunology
container_volume 150
creator Li, Duo
Zhang, Weiwei
Wang, Tong
Yang, Yang
Hua, Sijie
Ruan, Qingxin
Wang, Xi
Zhu, Chunhua
Meng, Zining
description Greater amberjack (Seriola dumerili) is a fish species that has significant economic and cultural value. It has a large size and grows rapidly. However, the intolerance to hypoxia poses a major obstacle to the growth of its aquaculture industry. This study focuses on the gills and spleen, two organs closely associated with the response to acute hypoxic stress. By simulating the acute hypoxic environment and using Illumina RNA-Seq technology, we explored the gills and spleen transcriptome changes in the acute hypoxia intolerant and tolerant groups of greater amberjack. It was discovered that gill tissues in the tolerant group may maintain a stable intracellular energy supply by promoting glycolysis and β-oxidation compared to the intolerant group. Additionally, it promotes angiogenesis, enhances the ability to absorb dissolved oxygen, and accelerates oxygen transport to the mitochondria, adapting to the hypoxic environment. Anti-apoptotic genes were up-regulated in gill tissues in the tolerant group compared to the intolerant group, thereby minimizing the damage of acute hypoxia. On the other hand, the spleen inhibited the TCA and energy-consuming lipid synthesis pathways to supply energy under acute hypoxic stress. Pro-angiogenic genes were down-regulated in the spleen of individuals in the tolerant group compared to the intolerant group, which may be related to organ function. The suppressed reactive oxygen species (ROS) production and the impaired immune response function of the spleen were also found. The study explored the acute hypoxic stress response in greater amberjack and the molecular mechanisms underlying its tolerance to acute hypoxia. •Key differentially expressed genes of gills and spleen related to acute hypoxia in Seriola dumerili were identified.•Gills of acute hypoxia-tolerant individuals promote glycolysis, β-oxidation, and angiogenesis.•Spleen of acute hypoxia-tolerant individuals inhibits tricarboxylic acid cycle, lipid synthesis, and glycolysis suppression.•Gills increase oxygen uptake, while the spleen releases blood cells to transport oxygen to tissues.
doi_str_mv 10.1016/j.fsi.2024.109602
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It has a large size and grows rapidly. However, the intolerance to hypoxia poses a major obstacle to the growth of its aquaculture industry. This study focuses on the gills and spleen, two organs closely associated with the response to acute hypoxic stress. By simulating the acute hypoxic environment and using Illumina RNA-Seq technology, we explored the gills and spleen transcriptome changes in the acute hypoxia intolerant and tolerant groups of greater amberjack. It was discovered that gill tissues in the tolerant group may maintain a stable intracellular energy supply by promoting glycolysis and β-oxidation compared to the intolerant group. Additionally, it promotes angiogenesis, enhances the ability to absorb dissolved oxygen, and accelerates oxygen transport to the mitochondria, adapting to the hypoxic environment. Anti-apoptotic genes were up-regulated in gill tissues in the tolerant group compared to the intolerant group, thereby minimizing the damage of acute hypoxia. On the other hand, the spleen inhibited the TCA and energy-consuming lipid synthesis pathways to supply energy under acute hypoxic stress. Pro-angiogenic genes were down-regulated in the spleen of individuals in the tolerant group compared to the intolerant group, which may be related to organ function. The suppressed reactive oxygen species (ROS) production and the impaired immune response function of the spleen were also found. The study explored the acute hypoxic stress response in greater amberjack and the molecular mechanisms underlying its tolerance to acute hypoxia. •Key differentially expressed genes of gills and spleen related to acute hypoxia in Seriola dumerili were identified.•Gills of acute hypoxia-tolerant individuals promote glycolysis, β-oxidation, and angiogenesis.•Spleen of acute hypoxia-tolerant individuals inhibits tricarboxylic acid cycle, lipid synthesis, and glycolysis suppression.•Gills increase oxygen uptake, while the spleen releases blood cells to transport oxygen to tissues.</description><identifier>ISSN: 1050-4648</identifier><identifier>EISSN: 1095-9947</identifier><identifier>DOI: 10.1016/j.fsi.2024.109602</identifier><identifier>PMID: 38729252</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>angiogenesis ; aquaculture industry ; dissolved oxygen ; energy ; fish ; gene expression ; Gills ; glycolysis ; Hypoxia ; immune response ; lipids ; mitochondria ; oxygen ; reactive oxygen species ; sequence analysis ; Seriola dumerili ; shellfish ; Spleen ; stress response ; Transcriptome</subject><ispartof>Fish &amp; shellfish immunology, 2024-07, Vol.150, p.109602-109602, Article 109602</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024 Elsevier Ltd. 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It has a large size and grows rapidly. However, the intolerance to hypoxia poses a major obstacle to the growth of its aquaculture industry. This study focuses on the gills and spleen, two organs closely associated with the response to acute hypoxic stress. By simulating the acute hypoxic environment and using Illumina RNA-Seq technology, we explored the gills and spleen transcriptome changes in the acute hypoxia intolerant and tolerant groups of greater amberjack. It was discovered that gill tissues in the tolerant group may maintain a stable intracellular energy supply by promoting glycolysis and β-oxidation compared to the intolerant group. Additionally, it promotes angiogenesis, enhances the ability to absorb dissolved oxygen, and accelerates oxygen transport to the mitochondria, adapting to the hypoxic environment. Anti-apoptotic genes were up-regulated in gill tissues in the tolerant group compared to the intolerant group, thereby minimizing the damage of acute hypoxia. On the other hand, the spleen inhibited the TCA and energy-consuming lipid synthesis pathways to supply energy under acute hypoxic stress. Pro-angiogenic genes were down-regulated in the spleen of individuals in the tolerant group compared to the intolerant group, which may be related to organ function. The suppressed reactive oxygen species (ROS) production and the impaired immune response function of the spleen were also found. The study explored the acute hypoxic stress response in greater amberjack and the molecular mechanisms underlying its tolerance to acute hypoxia. •Key differentially expressed genes of gills and spleen related to acute hypoxia in Seriola dumerili were identified.•Gills of acute hypoxia-tolerant individuals promote glycolysis, β-oxidation, and angiogenesis.•Spleen of acute hypoxia-tolerant individuals inhibits tricarboxylic acid cycle, lipid synthesis, and glycolysis suppression.•Gills increase oxygen uptake, while the spleen releases blood cells to transport oxygen to tissues.</description><subject>angiogenesis</subject><subject>aquaculture industry</subject><subject>dissolved oxygen</subject><subject>energy</subject><subject>fish</subject><subject>gene expression</subject><subject>Gills</subject><subject>glycolysis</subject><subject>Hypoxia</subject><subject>immune response</subject><subject>lipids</subject><subject>mitochondria</subject><subject>oxygen</subject><subject>reactive oxygen species</subject><subject>sequence analysis</subject><subject>Seriola dumerili</subject><subject>shellfish</subject><subject>Spleen</subject><subject>stress response</subject><subject>Transcriptome</subject><issn>1050-4648</issn><issn>1095-9947</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkUtPGzEUha2KqqS0P4AN8jIsJvV7POoKIWgqReoCurY89p3UwfOoPUHw7-sowJKu7rlX3zmLexA6p2RFCVXfdqsuhxUjTJS9UYR9QIsiZNU0oj45aEkqoYQ-RZ9z3hFCFFfkEzrlumYNk2yB_Pp5Gp-CxXlOkDO2cYaU8RYGwPA0HW5hHHAY8PwH8DbEWJjB4zxFgAGPHd4msMWDbd9C2ln3gJd3kMIYrd_3RcRw-QV97GzM8PVlnqHftzf31-tq8-vHz-urTeU413MlOqK8bFkrJLWi1mWo2mqrKJOd9p4pxZyzWtXSt85rpVrCPOma1sla05afoeUxd0rj3z3k2fQhO4jRDjDus-FUckUV4eT_KJG8qQUVqqD0iLo05pygM1MKvU3PhhJz6MHsTOnBHHowxx6K5-Ilft_24N8cr48vwPcjAOUfjwGSyS7A4MCHBG42fgzvxP8DuHWYOg</recordid><startdate>20240701</startdate><enddate>20240701</enddate><creator>Li, Duo</creator><creator>Zhang, Weiwei</creator><creator>Wang, Tong</creator><creator>Yang, Yang</creator><creator>Hua, Sijie</creator><creator>Ruan, Qingxin</creator><creator>Wang, Xi</creator><creator>Zhu, Chunhua</creator><creator>Meng, Zining</creator><general>Elsevier Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20240701</creationdate><title>Hypoxia stress alters gene expression in the gills and spleen of greater amberjack (Serioladumerili)</title><author>Li, Duo ; 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shellfish immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Li, Duo</au><au>Zhang, Weiwei</au><au>Wang, Tong</au><au>Yang, Yang</au><au>Hua, Sijie</au><au>Ruan, Qingxin</au><au>Wang, Xi</au><au>Zhu, Chunhua</au><au>Meng, Zining</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Hypoxia stress alters gene expression in the gills and spleen of greater amberjack (Serioladumerili)</atitle><jtitle>Fish &amp; shellfish immunology</jtitle><addtitle>Fish Shellfish Immunol</addtitle><date>2024-07-01</date><risdate>2024</risdate><volume>150</volume><spage>109602</spage><epage>109602</epage><pages>109602-109602</pages><artnum>109602</artnum><issn>1050-4648</issn><eissn>1095-9947</eissn><abstract>Greater amberjack (Seriola dumerili) is a fish species that has significant economic and cultural value. 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On the other hand, the spleen inhibited the TCA and energy-consuming lipid synthesis pathways to supply energy under acute hypoxic stress. Pro-angiogenic genes were down-regulated in the spleen of individuals in the tolerant group compared to the intolerant group, which may be related to organ function. The suppressed reactive oxygen species (ROS) production and the impaired immune response function of the spleen were also found. 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subjects angiogenesis
aquaculture industry
dissolved oxygen
energy
fish
gene expression
Gills
glycolysis
Hypoxia
immune response
lipids
mitochondria
oxygen
reactive oxygen species
sequence analysis
Seriola dumerili
shellfish
Spleen
stress response
Transcriptome
title Hypoxia stress alters gene expression in the gills and spleen of greater amberjack (Serioladumerili)
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