Temperature training improves transcriptional homeostasis after heat shock in juvenile Atlantic sturgeon (Acipenser oxyrinchus)
Exposure to high temperatures can lead to thermotolerance in fish, which is hypothesized to potentially improve post-release survival in species under restocking programs, like Atlantic sturgeon. The aim of this study was to determine whether Atlantic sturgeon juveniles exposed to a 4-week temperatu...
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Veröffentlicht in: | Fish physiology and biochemistry 2020-10, Vol.46 (5), p.1653-1664 |
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creator | Yebra-Pimentel, Elena Santidrián Reis, Bruno Gessner, Jörn Wuertz, Sven Dirks, Ron P. H. |
description | Exposure to high temperatures can lead to thermotolerance in fish, which is hypothesized to potentially improve post-release survival in species under restocking programs, like Atlantic sturgeon. The aim of this study was to determine whether Atlantic sturgeon juveniles exposed to a 4-week temperature treatment respond differently to a subsequent heat shock than juveniles exposed to heat shock for the first time (naive fish). Response to heat shock was assessed by mapping the liver transcriptome. In total, 838 unique contigs were differentially expressed between the trained and the control group (592 downregulated, 261 upregulated, and 15 down- or upregulated, depending on the condition), corresponding to genes involved in the response to heat, tissue damage, proteolysis, and metabolism. Temperature-trained fish showed 2–4-fold fewer dysregulated contigs than naive fish, indicating their ability to maintain and recover homeostasis faster. During heat shock,
hspc1
was upregulated in both experimental groups, while
hspa1
and
dnaja4
were exclusively upregulated in the control. Overall, compensatory mechanisms were observed in addition to the heat shock response. Only two genes,
fgg
and
apnl
, were upregulated at nearly all timepoints in both groups. Peptidases were more strongly downregulated in control fish, which also showed a reduction in lipid metabolism during recovery. Keratins,
pck1
,
gadd45ga
, and
gadd45gb
were differentially expressed between trained and control fish, and due to their roles in tissue protection and ER stress reduction, they might be responsible for the maintenance of the transcriptional homeostasis observed in trained fish. |
doi_str_mv | 10.1007/s10695-020-00818-4 |
format | Article |
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hspc1
was upregulated in both experimental groups, while
hspa1
and
dnaja4
were exclusively upregulated in the control. Overall, compensatory mechanisms were observed in addition to the heat shock response. Only two genes,
fgg
and
apnl
, were upregulated at nearly all timepoints in both groups. Peptidases were more strongly downregulated in control fish, which also showed a reduction in lipid metabolism during recovery. Keratins,
pck1
,
gadd45ga
, and
gadd45gb
were differentially expressed between trained and control fish, and due to their roles in tissue protection and ER stress reduction, they might be responsible for the maintenance of the transcriptional homeostasis observed in trained fish.</description><identifier>ISSN: 0920-1742</identifier><identifier>EISSN: 1573-5168</identifier><identifier>DOI: 10.1007/s10695-020-00818-4</identifier><identifier>PMID: 32583280</identifier><language>eng</language><publisher>Dordrecht: Springer Netherlands</publisher><subject>Acipenser oxyrinchus oxyrinchus ; Adaptation, Physiological ; Animal Anatomy ; Animal Biochemistry ; Animal Physiology ; Animals ; Biomedical and Life Sciences ; Control ; Exposure ; Fish ; Fishes - physiology ; Freshwater & Marine Ecology ; Freshwater fishes ; Gene expression ; Gene Expression Regulation - physiology ; Gene mapping ; Genes ; Heat ; Heat shock ; Heat-Shock Response ; High temperature ; Histology ; Homeostasis ; Juveniles ; Keratin ; Life Sciences ; Lipid metabolism ; Lipids ; Mapping ; Metabolism ; Morphology ; Peptidases ; Proteolysis ; Reduction ; Restocking ; Sturgeon ; Survival ; Temperature ; Temperature tolerance ; Tissue ; Training ; Transcription ; Zoology</subject><ispartof>Fish physiology and biochemistry, 2020-10, Vol.46 (5), p.1653-1664</ispartof><rights>Springer Nature B.V. 2020</rights><rights>Springer Nature B.V. 2020.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-e8142ce641fbaea00d4a9053d686fba3bcee32fdac1f9ae902d00bd441554fc43</citedby><cites>FETCH-LOGICAL-c375t-e8142ce641fbaea00d4a9053d686fba3bcee32fdac1f9ae902d00bd441554fc43</cites><orcidid>0000-0002-9645-2364</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s10695-020-00818-4$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s10695-020-00818-4$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32583280$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yebra-Pimentel, Elena Santidrián</creatorcontrib><creatorcontrib>Reis, Bruno</creatorcontrib><creatorcontrib>Gessner, Jörn</creatorcontrib><creatorcontrib>Wuertz, Sven</creatorcontrib><creatorcontrib>Dirks, Ron P. H.</creatorcontrib><title>Temperature training improves transcriptional homeostasis after heat shock in juvenile Atlantic sturgeon (Acipenser oxyrinchus)</title><title>Fish physiology and biochemistry</title><addtitle>Fish Physiol Biochem</addtitle><addtitle>Fish Physiol Biochem</addtitle><description>Exposure to high temperatures can lead to thermotolerance in fish, which is hypothesized to potentially improve post-release survival in species under restocking programs, like Atlantic sturgeon. The aim of this study was to determine whether Atlantic sturgeon juveniles exposed to a 4-week temperature treatment respond differently to a subsequent heat shock than juveniles exposed to heat shock for the first time (naive fish). Response to heat shock was assessed by mapping the liver transcriptome. In total, 838 unique contigs were differentially expressed between the trained and the control group (592 downregulated, 261 upregulated, and 15 down- or upregulated, depending on the condition), corresponding to genes involved in the response to heat, tissue damage, proteolysis, and metabolism. Temperature-trained fish showed 2–4-fold fewer dysregulated contigs than naive fish, indicating their ability to maintain and recover homeostasis faster. During heat shock,
hspc1
was upregulated in both experimental groups, while
hspa1
and
dnaja4
were exclusively upregulated in the control. Overall, compensatory mechanisms were observed in addition to the heat shock response. Only two genes,
fgg
and
apnl
, were upregulated at nearly all timepoints in both groups. Peptidases were more strongly downregulated in control fish, which also showed a reduction in lipid metabolism during recovery. Keratins,
pck1
,
gadd45ga
, and
gadd45gb
were differentially expressed between trained and control fish, and due to their roles in tissue protection and ER stress reduction, they might be responsible for the maintenance of the transcriptional homeostasis observed in trained fish.</description><subject>Acipenser oxyrinchus oxyrinchus</subject><subject>Adaptation, Physiological</subject><subject>Animal Anatomy</subject><subject>Animal Biochemistry</subject><subject>Animal Physiology</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Control</subject><subject>Exposure</subject><subject>Fish</subject><subject>Fishes - physiology</subject><subject>Freshwater & Marine Ecology</subject><subject>Freshwater fishes</subject><subject>Gene expression</subject><subject>Gene Expression Regulation - physiology</subject><subject>Gene mapping</subject><subject>Genes</subject><subject>Heat</subject><subject>Heat shock</subject><subject>Heat-Shock Response</subject><subject>High temperature</subject><subject>Histology</subject><subject>Homeostasis</subject><subject>Juveniles</subject><subject>Keratin</subject><subject>Life Sciences</subject><subject>Lipid metabolism</subject><subject>Lipids</subject><subject>Mapping</subject><subject>Metabolism</subject><subject>Morphology</subject><subject>Peptidases</subject><subject>Proteolysis</subject><subject>Reduction</subject><subject>Restocking</subject><subject>Sturgeon</subject><subject>Survival</subject><subject>Temperature</subject><subject>Temperature tolerance</subject><subject>Tissue</subject><subject>Training</subject><subject>Transcription</subject><subject>Zoology</subject><issn>0920-1742</issn><issn>1573-5168</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kcluFDEQhi0EIpPAC3BAlrgkh4by1stxFLFJkbiEc8vjrp7x0G0PLneUnHh1PEwAiQOnkqq--mv5GXsl4K0AaN6RgLozFUioAFrRVvoJWwnTqMqIun3KVtCVkmi0PGPnRHsA6JpaPGdnSppWyRZW7MctzgdMNi8JeU7WBx-23M-HFO-QjplALvlD9jHYie_ijJGyJU_cjhkT36HNnHbRfeM-8P1yh8FPyNd5siF7x6kobzEGfrl2_oCBSk-8f0g-uN1CVy_Ys9FOhC8f4wX7-uH97fWn6ubLx8_X65vKqcbkCluhpcNai3Fj0QIM2nZg1FC3dcmojUNUchysE2NnsQM5AGwGrYUxenRaXbDLk2457PuClPvZk8OpbIlxoV7q8ifQnagL-uYfdB-XVK4_UkoL3RhpCiVPlEuRKOHYH5KfbXroBfRHe_qTPX2xp_9lT3_c4vWj9LKZcfjT8tuPAqgTQKUUtpj-zv6P7E-oyZ5P</recordid><startdate>20201001</startdate><enddate>20201001</enddate><creator>Yebra-Pimentel, Elena Santidrián</creator><creator>Reis, Bruno</creator><creator>Gessner, Jörn</creator><creator>Wuertz, Sven</creator><creator>Dirks, Ron P. 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H.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-e8142ce641fbaea00d4a9053d686fba3bcee32fdac1f9ae902d00bd441554fc43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Acipenser oxyrinchus oxyrinchus</topic><topic>Adaptation, Physiological</topic><topic>Animal Anatomy</topic><topic>Animal Biochemistry</topic><topic>Animal Physiology</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Control</topic><topic>Exposure</topic><topic>Fish</topic><topic>Fishes - physiology</topic><topic>Freshwater & Marine Ecology</topic><topic>Freshwater fishes</topic><topic>Gene expression</topic><topic>Gene Expression Regulation - physiology</topic><topic>Gene mapping</topic><topic>Genes</topic><topic>Heat</topic><topic>Heat shock</topic><topic>Heat-Shock Response</topic><topic>High temperature</topic><topic>Histology</topic><topic>Homeostasis</topic><topic>Juveniles</topic><topic>Keratin</topic><topic>Life Sciences</topic><topic>Lipid metabolism</topic><topic>Lipids</topic><topic>Mapping</topic><topic>Metabolism</topic><topic>Morphology</topic><topic>Peptidases</topic><topic>Proteolysis</topic><topic>Reduction</topic><topic>Restocking</topic><topic>Sturgeon</topic><topic>Survival</topic><topic>Temperature</topic><topic>Temperature tolerance</topic><topic>Tissue</topic><topic>Training</topic><topic>Transcription</topic><topic>Zoology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yebra-Pimentel, Elena Santidrián</creatorcontrib><creatorcontrib>Reis, Bruno</creatorcontrib><creatorcontrib>Gessner, Jörn</creatorcontrib><creatorcontrib>Wuertz, Sven</creatorcontrib><creatorcontrib>Dirks, Ron P. 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H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Temperature training improves transcriptional homeostasis after heat shock in juvenile Atlantic sturgeon (Acipenser oxyrinchus)</atitle><jtitle>Fish physiology and biochemistry</jtitle><stitle>Fish Physiol Biochem</stitle><addtitle>Fish Physiol Biochem</addtitle><date>2020-10-01</date><risdate>2020</risdate><volume>46</volume><issue>5</issue><spage>1653</spage><epage>1664</epage><pages>1653-1664</pages><issn>0920-1742</issn><eissn>1573-5168</eissn><abstract>Exposure to high temperatures can lead to thermotolerance in fish, which is hypothesized to potentially improve post-release survival in species under restocking programs, like Atlantic sturgeon. The aim of this study was to determine whether Atlantic sturgeon juveniles exposed to a 4-week temperature treatment respond differently to a subsequent heat shock than juveniles exposed to heat shock for the first time (naive fish). Response to heat shock was assessed by mapping the liver transcriptome. In total, 838 unique contigs were differentially expressed between the trained and the control group (592 downregulated, 261 upregulated, and 15 down- or upregulated, depending on the condition), corresponding to genes involved in the response to heat, tissue damage, proteolysis, and metabolism. Temperature-trained fish showed 2–4-fold fewer dysregulated contigs than naive fish, indicating their ability to maintain and recover homeostasis faster. During heat shock,
hspc1
was upregulated in both experimental groups, while
hspa1
and
dnaja4
were exclusively upregulated in the control. Overall, compensatory mechanisms were observed in addition to the heat shock response. Only two genes,
fgg
and
apnl
, were upregulated at nearly all timepoints in both groups. Peptidases were more strongly downregulated in control fish, which also showed a reduction in lipid metabolism during recovery. Keratins,
pck1
,
gadd45ga
, and
gadd45gb
were differentially expressed between trained and control fish, and due to their roles in tissue protection and ER stress reduction, they might be responsible for the maintenance of the transcriptional homeostasis observed in trained fish.</abstract><cop>Dordrecht</cop><pub>Springer Netherlands</pub><pmid>32583280</pmid><doi>10.1007/s10695-020-00818-4</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-9645-2364</orcidid></addata></record> |
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language | eng |
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subjects | Acipenser oxyrinchus oxyrinchus Adaptation, Physiological Animal Anatomy Animal Biochemistry Animal Physiology Animals Biomedical and Life Sciences Control Exposure Fish Fishes - physiology Freshwater & Marine Ecology Freshwater fishes Gene expression Gene Expression Regulation - physiology Gene mapping Genes Heat Heat shock Heat-Shock Response High temperature Histology Homeostasis Juveniles Keratin Life Sciences Lipid metabolism Lipids Mapping Metabolism Morphology Peptidases Proteolysis Reduction Restocking Sturgeon Survival Temperature Temperature tolerance Tissue Training Transcription Zoology |
title | Temperature training improves transcriptional homeostasis after heat shock in juvenile Atlantic sturgeon (Acipenser oxyrinchus) |
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