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Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii)

BACKGROUND: Maintaining osmotic equilibrium plays an important role in the survival of cold-water fishes. Heat stress has been proven to reduce the activity of Na(+)/K(+)-ATPase in the gill tissue, leading to destruction of the osmotic equilibrium. However, the mechanism of megatemperature affecting...

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Autores principales: Yang, Shiyong, Li, Datian, Feng, Langkun, Zhang, Chaoyang, Xi, Dandan, Liu, Hongli, Yan, Chaozhan, Xu, Zihan, Zhang, Yujie, Li, Yunkun, Yan, Taiming, He, Zhi, Wu, Jiayun, Gong, Quan, Du, Jun, Huang, Xiaoli, Du, Xiaogang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9809011/
https://www.ncbi.nlm.nih.gov/pubmed/36597034
http://dx.doi.org/10.1186/s12864-022-08969-9
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author Yang, Shiyong
Li, Datian
Feng, Langkun
Zhang, Chaoyang
Xi, Dandan
Liu, Hongli
Yan, Chaozhan
Xu, Zihan
Zhang, Yujie
Li, Yunkun
Yan, Taiming
He, Zhi
Wu, Jiayun
Gong, Quan
Du, Jun
Huang, Xiaoli
Du, Xiaogang
author_facet Yang, Shiyong
Li, Datian
Feng, Langkun
Zhang, Chaoyang
Xi, Dandan
Liu, Hongli
Yan, Chaozhan
Xu, Zihan
Zhang, Yujie
Li, Yunkun
Yan, Taiming
He, Zhi
Wu, Jiayun
Gong, Quan
Du, Jun
Huang, Xiaoli
Du, Xiaogang
author_sort Yang, Shiyong
collection PubMed
description BACKGROUND: Maintaining osmotic equilibrium plays an important role in the survival of cold-water fishes. Heat stress has been proven to reduce the activity of Na(+)/K(+)-ATPase in the gill tissue, leading to destruction of the osmotic equilibrium. However, the mechanism of megatemperature affecting gill osmoregulation has not been fully elucidated. RESULTS: In this study, Siberian sturgeon (Acipenser baerii) was used to analyze histopathological change, plasma ion level, and transcriptome of gill tissue subjected to 20℃, 24℃and 28℃. The results showed that ROS level and damage were increased in gill tissue with the increasing of heat stress temperature. Plasma Cl(−) level at 28℃ was distinctly lower than that at 20℃ and 24℃, while no significant difference was found in Na(+) and K(+) ion levels among different groups. Transcriptome analysis displayed that osmoregulation-, DNA-repair- and apoptosis-related terms or pathways were enriched in GO and KEGG analysis. Moreover, 194 osmoregulation-related genes were identified. Amongst, the expression of genes limiting ion outflow, occluding (OCLN), and ion absorption, solute carrier family 4, member 2 (AE2) solute carrier family 9, member 3 (NHE3) chloride channel 2 (CLC-2) were increased, while Na(+)/K(+)-ATPase alpha (NKA-a) expression was decreased after heat stress. CONCLUSIONS: This study reveals for the first time that the effect of heat stress on damage and osmotic regulation in gill tissue of cold-water fishes. Heat stress increases the permeability of fish’s gill tissue, and induces the gill tissue to keep ion balance through active ion absorption and passive ion outflow. Our study will contribute to research of global-warming-caused effects on cold-water fishes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08969-9.
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spelling pubmed-98090112023-01-04 Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii) Yang, Shiyong Li, Datian Feng, Langkun Zhang, Chaoyang Xi, Dandan Liu, Hongli Yan, Chaozhan Xu, Zihan Zhang, Yujie Li, Yunkun Yan, Taiming He, Zhi Wu, Jiayun Gong, Quan Du, Jun Huang, Xiaoli Du, Xiaogang BMC Genomics Research BACKGROUND: Maintaining osmotic equilibrium plays an important role in the survival of cold-water fishes. Heat stress has been proven to reduce the activity of Na(+)/K(+)-ATPase in the gill tissue, leading to destruction of the osmotic equilibrium. However, the mechanism of megatemperature affecting gill osmoregulation has not been fully elucidated. RESULTS: In this study, Siberian sturgeon (Acipenser baerii) was used to analyze histopathological change, plasma ion level, and transcriptome of gill tissue subjected to 20℃, 24℃and 28℃. The results showed that ROS level and damage were increased in gill tissue with the increasing of heat stress temperature. Plasma Cl(−) level at 28℃ was distinctly lower than that at 20℃ and 24℃, while no significant difference was found in Na(+) and K(+) ion levels among different groups. Transcriptome analysis displayed that osmoregulation-, DNA-repair- and apoptosis-related terms or pathways were enriched in GO and KEGG analysis. Moreover, 194 osmoregulation-related genes were identified. Amongst, the expression of genes limiting ion outflow, occluding (OCLN), and ion absorption, solute carrier family 4, member 2 (AE2) solute carrier family 9, member 3 (NHE3) chloride channel 2 (CLC-2) were increased, while Na(+)/K(+)-ATPase alpha (NKA-a) expression was decreased after heat stress. CONCLUSIONS: This study reveals for the first time that the effect of heat stress on damage and osmotic regulation in gill tissue of cold-water fishes. Heat stress increases the permeability of fish’s gill tissue, and induces the gill tissue to keep ion balance through active ion absorption and passive ion outflow. Our study will contribute to research of global-warming-caused effects on cold-water fishes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08969-9. BioMed Central 2023-01-03 /pmc/articles/PMC9809011/ /pubmed/36597034 http://dx.doi.org/10.1186/s12864-022-08969-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Yang, Shiyong
Li, Datian
Feng, Langkun
Zhang, Chaoyang
Xi, Dandan
Liu, Hongli
Yan, Chaozhan
Xu, Zihan
Zhang, Yujie
Li, Yunkun
Yan, Taiming
He, Zhi
Wu, Jiayun
Gong, Quan
Du, Jun
Huang, Xiaoli
Du, Xiaogang
Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii)
title Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii)
title_full Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii)
title_fullStr Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii)
title_full_unstemmed Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii)
title_short Transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in Siberian sturgeon (Acipenser baerii)
title_sort transcriptome analysis reveals the high temperature induced damage is a significant factor affecting the osmotic function of gill tissue in siberian sturgeon (acipenser baerii)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9809011/
https://www.ncbi.nlm.nih.gov/pubmed/36597034
http://dx.doi.org/10.1186/s12864-022-08969-9
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