Alterations in mitochondrial structure and function in response to environmental temperature changes in Apostichopus japonicus

Global temperatures have risen as a result of climate change, and the resulting warmer seawater will exert physiological stresses on many aquatic animals, including Apostichopus japonicus. It has been suggested that the sensitivity of aquatic poikilothermal animals to climate change is closely relat...

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Veröffentlicht in:Marine environmental research 2024-02, Vol.194, p.106330-106330, Article 106330
Hauptverfasser: Lu, Lixin, Yang, Yu, Shi, Guojun, He, Xiaohua, Xu, Xiaohui, Feng, Yanwei, Wang, Weijun, Li, Zan, Yang, Jianmin, Li, Bin, Sun, Guohua
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container_title Marine environmental research
container_volume 194
creator Lu, Lixin
Yang, Yu
Shi, Guojun
He, Xiaohua
Xu, Xiaohui
Feng, Yanwei
Wang, Weijun
Li, Zan
Yang, Jianmin
Li, Bin
Sun, Guohua
description Global temperatures have risen as a result of climate change, and the resulting warmer seawater will exert physiological stresses on many aquatic animals, including Apostichopus japonicus. It has been suggested that the sensitivity of aquatic poikilothermal animals to climate change is closely related to mitochondrial function. Therefore, understanding the interaction between elevated temperature and mitochondrial functioning is key to characterizing organisms’ responses to heat stress. However, little is known about the mitochondrial response to heat stress in A. japonicus. In this work, we investigated the morphological and functional changes of A. japonicus mitochondria under three representative temperatures, control temperature (18 °C), aestivation temperature (25 °C) and heat stress temperature (32 °C) temperatures using transmission electron microscopy (TEM) observation of mitochondrial morphology combined with proteomics and metabolomics techniques. The results showed that the mitochondrial morphology of A. japonicus was altered, with decreases in the number of mitochondrial cristae at 25 °C and mitochondrial lysis, fracture, and vacuolization at 32 °C. Proteomic and metabolomic analyses revealed 103 differentially expressed proteins and 161 differential metabolites at 25 °C. At 32 °C, the levels of 214 proteins and 172 metabolites were significantly altered. These proteins and metabolites were involved in the tricarboxylic acid (TCA) cycle, substance transport, membrane potential homeostasis, anti-stress processes, mitochondrial autophagy, and apoptosis. Furthermore, a hypothetical network of proteins and metabolites in A. japonicus mitochondria in response to temperature changes was constructed based on proteomic and metabolomic data. These results suggest that the dynamic regulation of mitochondrial energy metabolism, resistance to oxidative stress, autophagy, apoptosis, and mitochondrial morphology in A. japonicus may play important roles in the response to elevated temperatures. In summary, this study describes the response of A. japonicus mitochondria to temperature changes from the perspectives of morphology, proteins, and metabolites, which provided a better understanding the mechanisms of mitochondrial regulation under environment stress in marine echinoderms. [Display omitted] •Mitochondria were the focus of exploring the response of A. japonicus to heat stress.•Morphology, proteomics and metabolomics indicated changes in mitochondria.•Re
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It has been suggested that the sensitivity of aquatic poikilothermal animals to climate change is closely related to mitochondrial function. Therefore, understanding the interaction between elevated temperature and mitochondrial functioning is key to characterizing organisms’ responses to heat stress. However, little is known about the mitochondrial response to heat stress in A. japonicus. In this work, we investigated the morphological and functional changes of A. japonicus mitochondria under three representative temperatures, control temperature (18 °C), aestivation temperature (25 °C) and heat stress temperature (32 °C) temperatures using transmission electron microscopy (TEM) observation of mitochondrial morphology combined with proteomics and metabolomics techniques. The results showed that the mitochondrial morphology of A. japonicus was altered, with decreases in the number of mitochondrial cristae at 25 °C and mitochondrial lysis, fracture, and vacuolization at 32 °C. Proteomic and metabolomic analyses revealed 103 differentially expressed proteins and 161 differential metabolites at 25 °C. At 32 °C, the levels of 214 proteins and 172 metabolites were significantly altered. These proteins and metabolites were involved in the tricarboxylic acid (TCA) cycle, substance transport, membrane potential homeostasis, anti-stress processes, mitochondrial autophagy, and apoptosis. Furthermore, a hypothetical network of proteins and metabolites in A. japonicus mitochondria in response to temperature changes was constructed based on proteomic and metabolomic data. These results suggest that the dynamic regulation of mitochondrial energy metabolism, resistance to oxidative stress, autophagy, apoptosis, and mitochondrial morphology in A. japonicus may play important roles in the response to elevated temperatures. In summary, this study describes the response of A. japonicus mitochondria to temperature changes from the perspectives of morphology, proteins, and metabolites, which provided a better understanding the mechanisms of mitochondrial regulation under environment stress in marine echinoderms. [Display omitted] •Mitochondria were the focus of exploring the response of A. japonicus to heat stress.•Morphology, proteomics and metabolomics indicated changes in mitochondria.•Regulation existed in oxidative stress, energy metabolism, and material transport.•A hypothesized network of proteins and metabolites in mitochondria was summarized.</description><identifier>ISSN: 0141-1136</identifier><identifier>EISSN: 1879-0291</identifier><identifier>DOI: 10.1016/j.marenvres.2023.106330</identifier><identifier>PMID: 38171258</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>ambient temperature ; apoptosis ; Apostichopus japonicus ; autophagy ; climate change ; energy metabolism ; estivation ; gene expression regulation ; heat stress ; High temperature stress ; homeostasis ; membrane potential ; metabolites ; Metabolomics ; Mitochondria ; oxidative stress ; Proteomic ; proteomics ; seawater ; transmission electron microscopy</subject><ispartof>Marine environmental research, 2024-02, Vol.194, p.106330-106330, Article 106330</ispartof><rights>2023 Elsevier Ltd</rights><rights>Copyright © 2023 Elsevier Ltd. 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It has been suggested that the sensitivity of aquatic poikilothermal animals to climate change is closely related to mitochondrial function. Therefore, understanding the interaction between elevated temperature and mitochondrial functioning is key to characterizing organisms’ responses to heat stress. However, little is known about the mitochondrial response to heat stress in A. japonicus. In this work, we investigated the morphological and functional changes of A. japonicus mitochondria under three representative temperatures, control temperature (18 °C), aestivation temperature (25 °C) and heat stress temperature (32 °C) temperatures using transmission electron microscopy (TEM) observation of mitochondrial morphology combined with proteomics and metabolomics techniques. The results showed that the mitochondrial morphology of A. japonicus was altered, with decreases in the number of mitochondrial cristae at 25 °C and mitochondrial lysis, fracture, and vacuolization at 32 °C. Proteomic and metabolomic analyses revealed 103 differentially expressed proteins and 161 differential metabolites at 25 °C. At 32 °C, the levels of 214 proteins and 172 metabolites were significantly altered. These proteins and metabolites were involved in the tricarboxylic acid (TCA) cycle, substance transport, membrane potential homeostasis, anti-stress processes, mitochondrial autophagy, and apoptosis. Furthermore, a hypothetical network of proteins and metabolites in A. japonicus mitochondria in response to temperature changes was constructed based on proteomic and metabolomic data. These results suggest that the dynamic regulation of mitochondrial energy metabolism, resistance to oxidative stress, autophagy, apoptosis, and mitochondrial morphology in A. japonicus may play important roles in the response to elevated temperatures. In summary, this study describes the response of A. japonicus mitochondria to temperature changes from the perspectives of morphology, proteins, and metabolites, which provided a better understanding the mechanisms of mitochondrial regulation under environment stress in marine echinoderms. [Display omitted] •Mitochondria were the focus of exploring the response of A. japonicus to heat stress.•Morphology, proteomics and metabolomics indicated changes in mitochondria.•Regulation existed in oxidative stress, energy metabolism, and material transport.•A hypothesized network of proteins and metabolites in mitochondria was summarized.</description><subject>ambient temperature</subject><subject>apoptosis</subject><subject>Apostichopus japonicus</subject><subject>autophagy</subject><subject>climate change</subject><subject>energy metabolism</subject><subject>estivation</subject><subject>gene expression regulation</subject><subject>heat stress</subject><subject>High temperature stress</subject><subject>homeostasis</subject><subject>membrane potential</subject><subject>metabolites</subject><subject>Metabolomics</subject><subject>Mitochondria</subject><subject>oxidative stress</subject><subject>Proteomic</subject><subject>proteomics</subject><subject>seawater</subject><subject>transmission electron microscopy</subject><issn>0141-1136</issn><issn>1879-0291</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqFkUFv3CAUhFHVqNls8hdaH3vxlgcGvMdVlCaRIuXSnhGLn7OsbHABR-olv724m-SaEwh9M4NmCPkGdAMU5I_jZjQR_XPEtGGU8fIqOaefyApata0p28JnsqLQQA3A5Tm5SOlIKRUKxBdyzltQwES7Ii-7IWM02QWfKuer0eVgD8F30ZmhSjnONs8RK-O7qp-9XcCFK8FTkWCVQ1X-4WLwI_pcNBnHaXFcVPZg_BP-N95NIWVXrKc5VUdTxM7O6ZKc9WZIePV6rsnvnze_ru_qh8fb--vdQ20b2uS6Y9gzCVbJvhWlgLbcsDccELhRUsBeNq1EqqRligLbd1wx2rLOSIWSGb4m30--Uwx_ZkxZjy5ZHAbjMcxJcxBcCLWV7YdoqZbCthFMFlSdUBtDShF7PUVXhvmrgeplJ33U7zvpZSd92qkov76GzPsRu3fd2zAF2J0ALK08O4w6WYfeYuci2qy74D4M-Qc7Narp</recordid><startdate>20240201</startdate><enddate>20240201</enddate><creator>Lu, Lixin</creator><creator>Yang, Yu</creator><creator>Shi, Guojun</creator><creator>He, Xiaohua</creator><creator>Xu, Xiaohui</creator><creator>Feng, Yanwei</creator><creator>Wang, Weijun</creator><creator>Li, Zan</creator><creator>Yang, Jianmin</creator><creator>Li, Bin</creator><creator>Sun, Guohua</creator><general>Elsevier Ltd</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><orcidid>https://orcid.org/0000-0002-6456-6893</orcidid></search><sort><creationdate>20240201</creationdate><title>Alterations in mitochondrial structure and function in response to environmental temperature changes in Apostichopus japonicus</title><author>Lu, Lixin ; 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It has been suggested that the sensitivity of aquatic poikilothermal animals to climate change is closely related to mitochondrial function. Therefore, understanding the interaction between elevated temperature and mitochondrial functioning is key to characterizing organisms’ responses to heat stress. However, little is known about the mitochondrial response to heat stress in A. japonicus. In this work, we investigated the morphological and functional changes of A. japonicus mitochondria under three representative temperatures, control temperature (18 °C), aestivation temperature (25 °C) and heat stress temperature (32 °C) temperatures using transmission electron microscopy (TEM) observation of mitochondrial morphology combined with proteomics and metabolomics techniques. The results showed that the mitochondrial morphology of A. japonicus was altered, with decreases in the number of mitochondrial cristae at 25 °C and mitochondrial lysis, fracture, and vacuolization at 32 °C. Proteomic and metabolomic analyses revealed 103 differentially expressed proteins and 161 differential metabolites at 25 °C. At 32 °C, the levels of 214 proteins and 172 metabolites were significantly altered. These proteins and metabolites were involved in the tricarboxylic acid (TCA) cycle, substance transport, membrane potential homeostasis, anti-stress processes, mitochondrial autophagy, and apoptosis. Furthermore, a hypothetical network of proteins and metabolites in A. japonicus mitochondria in response to temperature changes was constructed based on proteomic and metabolomic data. These results suggest that the dynamic regulation of mitochondrial energy metabolism, resistance to oxidative stress, autophagy, apoptosis, and mitochondrial morphology in A. japonicus may play important roles in the response to elevated temperatures. In summary, this study describes the response of A. japonicus mitochondria to temperature changes from the perspectives of morphology, proteins, and metabolites, which provided a better understanding the mechanisms of mitochondrial regulation under environment stress in marine echinoderms. [Display omitted] •Mitochondria were the focus of exploring the response of A. japonicus to heat stress.•Morphology, proteomics and metabolomics indicated changes in mitochondria.•Regulation existed in oxidative stress, energy metabolism, and material transport.•A hypothesized network of proteins and metabolites in mitochondria was summarized.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>38171258</pmid><doi>10.1016/j.marenvres.2023.106330</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-6456-6893</orcidid></addata></record>
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subjects ambient temperature
apoptosis
Apostichopus japonicus
autophagy
climate change
energy metabolism
estivation
gene expression regulation
heat stress
High temperature stress
homeostasis
membrane potential
metabolites
Metabolomics
Mitochondria
oxidative stress
Proteomic
proteomics
seawater
transmission electron microscopy
title Alterations in mitochondrial structure and function in response to environmental temperature changes in Apostichopus japonicus
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