Cargando…

Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts

BACKGROUND: Fish encounter oxidative stress several times during their lifetime, and it has a pervasive influence on their health and welfare. One of the triggers of oxidative stress in fish farming is the use of oxidative disinfectants to improve rearing conditions, especially in production systems...

Descripción completa

Detalles Bibliográficos
Autores principales: Osório, João, Stiller, Kevin T., Reiten, Britt-Kristin, Kolarevic, Jelena, Johansen, Lill-Heidi, Afonso, Fernando, Lazado, Carlo C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127346/
https://www.ncbi.nlm.nih.gov/pubmed/37170301
http://dx.doi.org/10.1186/s40850-021-00100-x
_version_ 1785030445801406464
author Osório, João
Stiller, Kevin T.
Reiten, Britt-Kristin
Kolarevic, Jelena
Johansen, Lill-Heidi
Afonso, Fernando
Lazado, Carlo C.
author_facet Osório, João
Stiller, Kevin T.
Reiten, Britt-Kristin
Kolarevic, Jelena
Johansen, Lill-Heidi
Afonso, Fernando
Lazado, Carlo C.
author_sort Osório, João
collection PubMed
description BACKGROUND: Fish encounter oxidative stress several times during their lifetime, and it has a pervasive influence on their health and welfare. One of the triggers of oxidative stress in fish farming is the use of oxidative disinfectants to improve rearing conditions, especially in production systems employing recirculation technology. Here we report the physiological and morphological adaptive responses of Atlantic salmon (Salmo salar L.) post-smolts to intermittent exposure to a potent oxidative agent peracetic acid (PAA). Fish reared in semi-commercial scale brackish water recirculating aquaculture system (RAS) were exposed to 1 ppm PAA every 3 days over 6 weeks. Mucosal and systemic responses were profiled before exposure, 22 and 45 days during the intermittent PAA administration. RESULTS: Oxidative stress was likely triggered as plasma antioxidant capacity increased significantly during the exposure period. Adaptive stress response to the periodic oxidant challenge was likewise demonstrated in the changes in plasma glucose and lactate levels. PAA-induced alterations in the transcription of antioxidants, cytokines, heat shock proteins and mucin genes showed a tissue-specific pattern: downregulation was observed in the gills and olfactory rosette, upregulation occurred in the skin, and no substantial changes in the liver. Further, PAA exposure resulted in histological changes in key mucosal organs (i.e. olfactory rosette, skin and gills); pathological alterations were predominant in the gills where cases of epithelial lifting, hypertrophy and clubbing were prevalent. In addition, intermittent PAA administration resulted in an apparent overproduction of mucus in the nasal mucosa. Lastly, PAA did not dramatically alter the ability of salmon to mount a physiological stress response in the presence of a secondary stressor, though some subtle interference was documented in the kinetics and magnitude of plasma cortisol and glucose response post-stress. CONCLUSIONS: The present study collectively demonstrated that intermittent oxidant exposure was a mild environmental stressor that salmon could mount strong adaptive responses at systemic and mucosal levels. The results will be valuable in optimising the rearing conditions of post-smolts in RAS, especially in adopting water treatment strategies that do not considerably interfere with fish health and welfare. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-021-00100-x.
format Online
Article
Text
id pubmed-10127346
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-101273462023-04-26 Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts Osório, João Stiller, Kevin T. Reiten, Britt-Kristin Kolarevic, Jelena Johansen, Lill-Heidi Afonso, Fernando Lazado, Carlo C. BMC Zool Research Article BACKGROUND: Fish encounter oxidative stress several times during their lifetime, and it has a pervasive influence on their health and welfare. One of the triggers of oxidative stress in fish farming is the use of oxidative disinfectants to improve rearing conditions, especially in production systems employing recirculation technology. Here we report the physiological and morphological adaptive responses of Atlantic salmon (Salmo salar L.) post-smolts to intermittent exposure to a potent oxidative agent peracetic acid (PAA). Fish reared in semi-commercial scale brackish water recirculating aquaculture system (RAS) were exposed to 1 ppm PAA every 3 days over 6 weeks. Mucosal and systemic responses were profiled before exposure, 22 and 45 days during the intermittent PAA administration. RESULTS: Oxidative stress was likely triggered as plasma antioxidant capacity increased significantly during the exposure period. Adaptive stress response to the periodic oxidant challenge was likewise demonstrated in the changes in plasma glucose and lactate levels. PAA-induced alterations in the transcription of antioxidants, cytokines, heat shock proteins and mucin genes showed a tissue-specific pattern: downregulation was observed in the gills and olfactory rosette, upregulation occurred in the skin, and no substantial changes in the liver. Further, PAA exposure resulted in histological changes in key mucosal organs (i.e. olfactory rosette, skin and gills); pathological alterations were predominant in the gills where cases of epithelial lifting, hypertrophy and clubbing were prevalent. In addition, intermittent PAA administration resulted in an apparent overproduction of mucus in the nasal mucosa. Lastly, PAA did not dramatically alter the ability of salmon to mount a physiological stress response in the presence of a secondary stressor, though some subtle interference was documented in the kinetics and magnitude of plasma cortisol and glucose response post-stress. CONCLUSIONS: The present study collectively demonstrated that intermittent oxidant exposure was a mild environmental stressor that salmon could mount strong adaptive responses at systemic and mucosal levels. The results will be valuable in optimising the rearing conditions of post-smolts in RAS, especially in adopting water treatment strategies that do not considerably interfere with fish health and welfare. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-021-00100-x. BioMed Central 2022-01-04 /pmc/articles/PMC10127346/ /pubmed/37170301 http://dx.doi.org/10.1186/s40850-021-00100-x Text en © The Author(s) 2021 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 Article
Osório, João
Stiller, Kevin T.
Reiten, Britt-Kristin
Kolarevic, Jelena
Johansen, Lill-Heidi
Afonso, Fernando
Lazado, Carlo C.
Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts
title Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts
title_full Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts
title_fullStr Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts
title_full_unstemmed Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts
title_short Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts
title_sort intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from atlantic salmon post-smolts
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127346/
https://www.ncbi.nlm.nih.gov/pubmed/37170301
http://dx.doi.org/10.1186/s40850-021-00100-x
work_keys_str_mv AT osoriojoao intermittentadministrationofperaceticacidisamildenvironmentalstressorthatelicitsmucosalandsystemicadaptiveresponsesfromatlanticsalmonpostsmolts
AT stillerkevint intermittentadministrationofperaceticacidisamildenvironmentalstressorthatelicitsmucosalandsystemicadaptiveresponsesfromatlanticsalmonpostsmolts
AT reitenbrittkristin intermittentadministrationofperaceticacidisamildenvironmentalstressorthatelicitsmucosalandsystemicadaptiveresponsesfromatlanticsalmonpostsmolts
AT kolarevicjelena intermittentadministrationofperaceticacidisamildenvironmentalstressorthatelicitsmucosalandsystemicadaptiveresponsesfromatlanticsalmonpostsmolts
AT johansenlillheidi intermittentadministrationofperaceticacidisamildenvironmentalstressorthatelicitsmucosalandsystemicadaptiveresponsesfromatlanticsalmonpostsmolts
AT afonsofernando intermittentadministrationofperaceticacidisamildenvironmentalstressorthatelicitsmucosalandsystemicadaptiveresponsesfromatlanticsalmonpostsmolts
AT lazadocarloc intermittentadministrationofperaceticacidisamildenvironmentalstressorthatelicitsmucosalandsystemicadaptiveresponsesfromatlanticsalmonpostsmolts