Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts
Peracetic acid (PAA) is an organic peroxide that produces free radicals, which contribute to its potent disinfection power. At therapeutic doses, PAA is considered a mild stressor that can trigger transient local and systemic oxidative stress in fish, but the resulting consequences in the brain have...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Elsevier
2022-01-01
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| Series: | Toxicology Reports |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2214750022001457 |
| _version_ | 1811178754532179968 |
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| author | Danilo Carletto Mette W. Breiland Sigurd Hytterød Gerrit Timmerhaus Carlo C. Lazado |
| author_facet | Danilo Carletto Mette W. Breiland Sigurd Hytterød Gerrit Timmerhaus Carlo C. Lazado |
| author_sort | Danilo Carletto |
| collection | DOAJ |
| description | Peracetic acid (PAA) is an organic peroxide that produces free radicals, which contribute to its potent disinfection power. At therapeutic doses, PAA is considered a mild stressor that can trigger transient local and systemic oxidative stress in fish, but the resulting consequences in the brain have yet to be identified. Therefore, we report the brain transcriptome of Atlantic salmon (Salmo salar) smolts that have been periodically exposed to PAA. Fish were treated three times (every 15 days) with PAA with either short (15 min) or long (30 min) exposure periods. After the third treatment, the whole brain was collected and subjected to biochemical and transcriptomic analyses. The level of reactive oxygen species in the brain was not significantly affected by recurrent PAA treatments. Microarray analysis was performed on the whole brain and revealed 205 differentially expressed genes (DEGs), regardless of the duration of the treatment. The short exposure duration had a more considerable impact on the brain transcriptome, correlating with 70% more DEGs than the long exposure. Strikingly, the brain transcriptome was characterised by the downregulation of gene expression, especially in the short exposure group, and around 82% of the identified DEGs were downregulated. Some of the highly affected genes were key molecules of the vasotocinergic and isotocinergic systems and the corticotropin-releasing factor signalling system, indicating interference of the stress axis but could also suggest an anxiolytic effect. In addition, there were alterations in genes involved in cellular metabolism and processing, signalling and trafficking, and innate immunity, which underscores the physiological changes in the brain following recurrent PAA treatment. Overall, the transcriptomic data reveal that recurrent oxidant treatment could influence brain functions, and although the magnitude was marginal, the alterations suggested neurological adaptations of fish to PAA as a potential chemical stressor. The results identify the risks of PAA, which would be valuable in drafting a framework for its empirically driven use in fish farming. |
| first_indexed | 2024-04-11T06:23:21Z |
| format | Article |
| id | doaj.art-c6a102eb2a6e4e82a767602eee3459cd |
| institution | Directory Open Access Journal |
| issn | 2214-7500 |
| language | English |
| last_indexed | 2024-04-11T06:23:21Z |
| publishDate | 2022-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Toxicology Reports |
| spelling | doaj.art-c6a102eb2a6e4e82a767602eee3459cd2022-12-22T04:40:28ZengElsevierToxicology Reports2214-75002022-01-01914611471Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smoltsDanilo Carletto0Mette W. Breiland1Sigurd Hytterød2Gerrit Timmerhaus3Carlo C. Lazado4Nofima, Norwegian Institute of Food, Fisheries and Aquaculture Research, 1433 Ås, Norway; Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, 98166S Agata-Messina, ItalyNofima, Norwegian Institute of Food, Fisheries and Aquaculture Research, 9019 Tromsø, NorwayNorwegian Veterinary Institute, PO Box 750, Sentrum, 0106 Oslo, NorwayNofima, Norwegian Institute of Food, Fisheries and Aquaculture Research, 1433 Ås, NorwayNofima, Norwegian Institute of Food, Fisheries and Aquaculture Research, 1433 Ås, Norway; Corresponding author.Peracetic acid (PAA) is an organic peroxide that produces free radicals, which contribute to its potent disinfection power. At therapeutic doses, PAA is considered a mild stressor that can trigger transient local and systemic oxidative stress in fish, but the resulting consequences in the brain have yet to be identified. Therefore, we report the brain transcriptome of Atlantic salmon (Salmo salar) smolts that have been periodically exposed to PAA. Fish were treated three times (every 15 days) with PAA with either short (15 min) or long (30 min) exposure periods. After the third treatment, the whole brain was collected and subjected to biochemical and transcriptomic analyses. The level of reactive oxygen species in the brain was not significantly affected by recurrent PAA treatments. Microarray analysis was performed on the whole brain and revealed 205 differentially expressed genes (DEGs), regardless of the duration of the treatment. The short exposure duration had a more considerable impact on the brain transcriptome, correlating with 70% more DEGs than the long exposure. Strikingly, the brain transcriptome was characterised by the downregulation of gene expression, especially in the short exposure group, and around 82% of the identified DEGs were downregulated. Some of the highly affected genes were key molecules of the vasotocinergic and isotocinergic systems and the corticotropin-releasing factor signalling system, indicating interference of the stress axis but could also suggest an anxiolytic effect. In addition, there were alterations in genes involved in cellular metabolism and processing, signalling and trafficking, and innate immunity, which underscores the physiological changes in the brain following recurrent PAA treatment. Overall, the transcriptomic data reveal that recurrent oxidant treatment could influence brain functions, and although the magnitude was marginal, the alterations suggested neurological adaptations of fish to PAA as a potential chemical stressor. The results identify the risks of PAA, which would be valuable in drafting a framework for its empirically driven use in fish farming.http://www.sciencedirect.com/science/article/pii/S2214750022001457AquacultureDisinfectionFish welfareOxidative stressReactive oxygen species |
| spellingShingle | Danilo Carletto Mette W. Breiland Sigurd Hytterød Gerrit Timmerhaus Carlo C. Lazado Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts Toxicology Reports Aquaculture Disinfection Fish welfare Oxidative stress Reactive oxygen species |
| title | Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts |
| title_full | Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts |
| title_fullStr | Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts |
| title_full_unstemmed | Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts |
| title_short | Recurrent oxidant treatment induces dysregulation in the brain transcriptome of Atlantic salmon (Salmo salar) smolts |
| title_sort | recurrent oxidant treatment induces dysregulation in the brain transcriptome of atlantic salmon salmo salar smolts |
| topic | Aquaculture Disinfection Fish welfare Oxidative stress Reactive oxygen species |
| url | http://www.sciencedirect.com/science/article/pii/S2214750022001457 |
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