Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar)

Hydrogen sulphide (H2S) is considered an immunotoxicant, and its presence in the water can influence the mucosal barrier functions of fish. However, there is a significant knowledge gap on how fish mucosa responds to low environmental H2S levels. The present study investigated the consequences of pr...

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Published in:Ecotoxicology and Environmental Safety
Main Authors: Juan Bosco Ara-Díaz, Julie Hansen Bergstedt, Nora Albaladejo-Riad, Muhammad Salman Malik, Øivind Andersen, Carlo C. Lazado
Format: Article in Journal/Newspaper
Language:English
Published: Elsevier 2024
Subjects:
Online Access:https://doi.org/10.1016/j.ecoenv.2024.116617
https://doaj.org/article/e9712400b4f44ea4b13070e3daffa72c
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spelling ftdoajarticles:oai:doaj.org/article:e9712400b4f44ea4b13070e3daffa72c 2024-09-15T17:56:09+00:00 Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar) Juan Bosco Ara-Díaz Julie Hansen Bergstedt Nora Albaladejo-Riad Muhammad Salman Malik Øivind Andersen Carlo C. Lazado 2024-08-01T00:00:00Z https://doi.org/10.1016/j.ecoenv.2024.116617 https://doaj.org/article/e9712400b4f44ea4b13070e3daffa72c EN eng Elsevier http://www.sciencedirect.com/science/article/pii/S0147651324006936 https://doaj.org/toc/0147-6513 0147-6513 doi:10.1016/j.ecoenv.2024.116617 https://doaj.org/article/e9712400b4f44ea4b13070e3daffa72c Ecotoxicology and Environmental Safety, Vol 281, Iss , Pp 116617- (2024) Aquaculture Fish health Mucosal immunity Metabolomics Sulphide toxicity Recirculating aquaculture system Environmental pollution TD172-193.5 Environmental sciences GE1-350 article 2024 ftdoajarticles https://doi.org/10.1016/j.ecoenv.2024.116617 2024-08-05T17:48:55Z Hydrogen sulphide (H2S) is considered an immunotoxicant, and its presence in the water can influence the mucosal barrier functions of fish. However, there is a significant knowledge gap on how fish mucosa responds to low environmental H2S levels. The present study investigated the consequences of prolonged exposure to sub-lethal levels of H2S on the mucosal defences of Atlantic salmon (Salmo salar). Fish were continuously exposed to two levels of H2S (low: 0.05 µM; and high: 0.12 µM) for 12 days. Unexposed fish served as control. Molecular and histological profiling focused on the changes in the skin, gills and olfactory rosette. In addition, metabolomics and proteomics were performed on the skin and gill mucus. The gene expression profile indicated that the gills and olfactory rosette were more sensitive to H2S than the skin. The olfactory rosette showed a dose-dependent response, but not the gills. Genes related to stress responses were triggered at mucosal sites by H2S. Moreover, H2S elicited strong inflammatory responses, particularly in the gills. All mucosal organs demonstrated the key molecular repertoire for sulphide detoxification, but their temporal and spatial expression was not substantially affected by sub-lethal H2S levels. Mucosal barrier integrity was not considerably affected by H2S. Mucus metabolomes of the skin and gills were unaffected, but a matrix-dependent response was identified. Comparing the high-concentration group's skin and gills mucus metabolomes identified altered amino acid biosynthesis and metabolism pathways. The skin and gill mucus exhibited distinct proteomic profiles. Enrichment analysis revealed that proteins related to immunity and metabolism were affected in both mucus matrices. The present study expands our knowledge of the defence mechanisms against H2S at mucosal sites in Atlantic salmon. The findings offer insights into the health and welfare consequences of sub-lethal H2S, which can be incorporated into the risk assessment protocols in salmon land-based farms. Article in Journal/Newspaper Atlantic salmon Salmo salar Directory of Open Access Journals: DOAJ Articles Ecotoxicology and Environmental Safety 281 116617
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Aquaculture
Fish health
Mucosal immunity
Metabolomics
Sulphide toxicity
Recirculating aquaculture system
Environmental pollution
TD172-193.5
Environmental sciences
GE1-350
spellingShingle Aquaculture
Fish health
Mucosal immunity
Metabolomics
Sulphide toxicity
Recirculating aquaculture system
Environmental pollution
TD172-193.5
Environmental sciences
GE1-350
Juan Bosco Ara-Díaz
Julie Hansen Bergstedt
Nora Albaladejo-Riad
Muhammad Salman Malik
Øivind Andersen
Carlo C. Lazado
Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar)
topic_facet Aquaculture
Fish health
Mucosal immunity
Metabolomics
Sulphide toxicity
Recirculating aquaculture system
Environmental pollution
TD172-193.5
Environmental sciences
GE1-350
description Hydrogen sulphide (H2S) is considered an immunotoxicant, and its presence in the water can influence the mucosal barrier functions of fish. However, there is a significant knowledge gap on how fish mucosa responds to low environmental H2S levels. The present study investigated the consequences of prolonged exposure to sub-lethal levels of H2S on the mucosal defences of Atlantic salmon (Salmo salar). Fish were continuously exposed to two levels of H2S (low: 0.05 µM; and high: 0.12 µM) for 12 days. Unexposed fish served as control. Molecular and histological profiling focused on the changes in the skin, gills and olfactory rosette. In addition, metabolomics and proteomics were performed on the skin and gill mucus. The gene expression profile indicated that the gills and olfactory rosette were more sensitive to H2S than the skin. The olfactory rosette showed a dose-dependent response, but not the gills. Genes related to stress responses were triggered at mucosal sites by H2S. Moreover, H2S elicited strong inflammatory responses, particularly in the gills. All mucosal organs demonstrated the key molecular repertoire for sulphide detoxification, but their temporal and spatial expression was not substantially affected by sub-lethal H2S levels. Mucosal barrier integrity was not considerably affected by H2S. Mucus metabolomes of the skin and gills were unaffected, but a matrix-dependent response was identified. Comparing the high-concentration group's skin and gills mucus metabolomes identified altered amino acid biosynthesis and metabolism pathways. The skin and gill mucus exhibited distinct proteomic profiles. Enrichment analysis revealed that proteins related to immunity and metabolism were affected in both mucus matrices. The present study expands our knowledge of the defence mechanisms against H2S at mucosal sites in Atlantic salmon. The findings offer insights into the health and welfare consequences of sub-lethal H2S, which can be incorporated into the risk assessment protocols in salmon land-based farms.
format Article in Journal/Newspaper
author Juan Bosco Ara-Díaz
Julie Hansen Bergstedt
Nora Albaladejo-Riad
Muhammad Salman Malik
Øivind Andersen
Carlo C. Lazado
author_facet Juan Bosco Ara-Díaz
Julie Hansen Bergstedt
Nora Albaladejo-Riad
Muhammad Salman Malik
Øivind Andersen
Carlo C. Lazado
author_sort Juan Bosco Ara-Díaz
title Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar)
title_short Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar)
title_full Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar)
title_fullStr Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar)
title_full_unstemmed Mucosal organs exhibit distinct response signatures to hydrogen sulphide in Atlantic salmon (Salmo salar)
title_sort mucosal organs exhibit distinct response signatures to hydrogen sulphide in atlantic salmon (salmo salar)
publisher Elsevier
publishDate 2024
url https://doi.org/10.1016/j.ecoenv.2024.116617
https://doaj.org/article/e9712400b4f44ea4b13070e3daffa72c
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Ecotoxicology and Environmental Safety, Vol 281, Iss , Pp 116617- (2024)
op_relation http://www.sciencedirect.com/science/article/pii/S0147651324006936
https://doaj.org/toc/0147-6513
0147-6513
doi:10.1016/j.ecoenv.2024.116617
https://doaj.org/article/e9712400b4f44ea4b13070e3daffa72c
op_doi https://doi.org/10.1016/j.ecoenv.2024.116617
container_title Ecotoxicology and Environmental Safety
container_volume 281
container_start_page 116617
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