Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximus

In recirculating aquaculture systems (RAS), the impact of dissolved oxygen (DO) fluctuations on turbot is still not fully understood. This study investigated these impacts by selecting 135 turbot (average dry weight: 6.0 ± 0.5 g) and exposing them to three DO levels: hypoxia (4.0 ± 0.5 mg/L), normox...

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Main Authors: Yi Chen, Yuntian Zhang, Rongwei Zhang, Hongsheng Deng, Xiangyu Meng, Kotoya Inaba, Tatsu Osato, Xiaoran Zhao, Yuzhe Han, Tongjun Ren
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Marine Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fmars.2024.1515112/full
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author Yi Chen
Yuntian Zhang
Rongwei Zhang
Hongsheng Deng
Xiangyu Meng
Kotoya Inaba
Tatsu Osato
Xiaoran Zhao
Xiaoran Zhao
Yuzhe Han
Yuzhe Han
Tongjun Ren
Tongjun Ren
author_facet Yi Chen
Yuntian Zhang
Rongwei Zhang
Hongsheng Deng
Xiangyu Meng
Kotoya Inaba
Tatsu Osato
Xiaoran Zhao
Xiaoran Zhao
Yuzhe Han
Yuzhe Han
Tongjun Ren
Tongjun Ren
author_sort Yi Chen
collection DOAJ
description In recirculating aquaculture systems (RAS), the impact of dissolved oxygen (DO) fluctuations on turbot is still not fully understood. This study investigated these impacts by selecting 135 turbot (average dry weight: 6.0 ± 0.5 g) and exposing them to three DO levels: hypoxia (4.0 ± 0.5 mg/L), normoxia (7.5 ± 0.5 mg/L), and hyperoxia (23.5 ± 0.5 mg/L). These groups were labeled as LF (low oxygen), NF (normal oxygen), and HF (high oxygen). The study aimed to explore the adaptive mechanisms of turbot under hypoxic and hyperoxic conditions, using microbiome, transcriptome, and hematological analyses over a 40-day period. The results suggest that hyperoxia significantly enhances turbot growth without compromising the composition of intestinal microbiome, whereas hypoxia markedly impairs growth and induces alterations in intestinal microbiome. Transcriptomic analysis revealed various pathways implicated in adaptation to both hypoxic and hyperoxic conditions, encompassing amino acid metabolism, protein metabolism, lipid metabolism, carbohydrate metabolism, the PPAR signaling pathway, etc. However, pathway changes are not completely consistent. For instance, pancreatic secretion is crucial for hyperoxia adaptation, while the HIF1α pathway plays a key role in hypoxia adaptation and tissue repair. Furthermore, genes ATP6, HIF1, HSP90, and CYP450 exhibited high expression levels during hypoxia, whereas Hbae5 and Man-SL showed elevated expression during hyperoxia. In hematological indicators, there are ways to help adapt to hypoxia and hyperoxia, including increased red blood cell (RBC) and hemoglobin (HGB) counts; gas and ion balance; elevated blood urea nitrogen (BUN) and malondialdehyde (MDA); increased polyphenol oxidase (PPO) and lysozyme (LZM) activity. Although turbot have adaptive mechanisms to both hypoxia and hyperoxia, extended exposure to hypoxia detrimentally affects growth, whereas hyperoxia facilitates it. These findings provide significant insights into the adaptive mechanisms of turbot in response to fluctuating DO levels.
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series Frontiers in Marine Science
spelling doaj-art-0b9b4c6dd1464213a29952c5746135ba2025-01-09T11:55:52ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452024-12-011110.3389/fmars.2024.15151121515112Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximusYi Chen0Yuntian Zhang1Rongwei Zhang2Hongsheng Deng3Xiangyu Meng4Kotoya Inaba5Tatsu Osato6Xiaoran Zhao7Xiaoran Zhao8Yuzhe Han9Yuzhe Han10Tongjun Ren11Tongjun Ren12College of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaIndustry gas devision, Iwatani Co., Ltd., Japan, Tokyo, JapanIndustry gas devision, Iwatani Co., Ltd., Japan, Tokyo, JapanCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaDalian Key Laboratory of Breeding, Reproduction and Aquaculture of Crustaceans, Dalian Ocean University, Dalian, Liaoning, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaDalian Key Laboratory of Breeding, Reproduction and Aquaculture of Crustaceans, Dalian Ocean University, Dalian, Liaoning, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, Liaoning, ChinaDalian Key Laboratory of Breeding, Reproduction and Aquaculture of Crustaceans, Dalian Ocean University, Dalian, Liaoning, ChinaIn recirculating aquaculture systems (RAS), the impact of dissolved oxygen (DO) fluctuations on turbot is still not fully understood. This study investigated these impacts by selecting 135 turbot (average dry weight: 6.0 ± 0.5 g) and exposing them to three DO levels: hypoxia (4.0 ± 0.5 mg/L), normoxia (7.5 ± 0.5 mg/L), and hyperoxia (23.5 ± 0.5 mg/L). These groups were labeled as LF (low oxygen), NF (normal oxygen), and HF (high oxygen). The study aimed to explore the adaptive mechanisms of turbot under hypoxic and hyperoxic conditions, using microbiome, transcriptome, and hematological analyses over a 40-day period. The results suggest that hyperoxia significantly enhances turbot growth without compromising the composition of intestinal microbiome, whereas hypoxia markedly impairs growth and induces alterations in intestinal microbiome. Transcriptomic analysis revealed various pathways implicated in adaptation to both hypoxic and hyperoxic conditions, encompassing amino acid metabolism, protein metabolism, lipid metabolism, carbohydrate metabolism, the PPAR signaling pathway, etc. However, pathway changes are not completely consistent. For instance, pancreatic secretion is crucial for hyperoxia adaptation, while the HIF1α pathway plays a key role in hypoxia adaptation and tissue repair. Furthermore, genes ATP6, HIF1, HSP90, and CYP450 exhibited high expression levels during hypoxia, whereas Hbae5 and Man-SL showed elevated expression during hyperoxia. In hematological indicators, there are ways to help adapt to hypoxia and hyperoxia, including increased red blood cell (RBC) and hemoglobin (HGB) counts; gas and ion balance; elevated blood urea nitrogen (BUN) and malondialdehyde (MDA); increased polyphenol oxidase (PPO) and lysozyme (LZM) activity. Although turbot have adaptive mechanisms to both hypoxia and hyperoxia, extended exposure to hypoxia detrimentally affects growth, whereas hyperoxia facilitates it. These findings provide significant insights into the adaptive mechanisms of turbot in response to fluctuating DO levels.https://www.frontiersin.org/articles/10.3389/fmars.2024.1515112/fullScophthalmus maximushypoxiahyperoxiaoxygen nanobubblesRAS
spellingShingle Yi Chen
Yuntian Zhang
Rongwei Zhang
Hongsheng Deng
Xiangyu Meng
Kotoya Inaba
Tatsu Osato
Xiaoran Zhao
Xiaoran Zhao
Yuzhe Han
Yuzhe Han
Tongjun Ren
Tongjun Ren
Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximus
Frontiers in Marine Science
Scophthalmus maximus
hypoxia
hyperoxia
oxygen nanobubbles
RAS
title Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximus
title_full Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximus
title_fullStr Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximus
title_full_unstemmed Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximus
title_short Adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot, Scophthalmus maximus
title_sort adaptive mechanisms to hypoxia and hyperoxia in juvenile turbot scophthalmus maximus
topic Scophthalmus maximus
hypoxia
hyperoxia
oxygen nanobubbles
RAS
url https://www.frontiersin.org/articles/10.3389/fmars.2024.1515112/full
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