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Early life stress causes persistent impacts on the microbiome of Atlantic salmon

Tamsyn Uren Webster Orcid Logo, S Consuegra del Olmo Orcid Logo, Carlos Garcia De Leaniz Orcid Logo

Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, Volume: 40, Start page: 100888

Swansea University Authors: Tamsyn Uren Webster Orcid Logo, S Consuegra del Olmo Orcid Logo, Carlos Garcia De Leaniz Orcid Logo

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Abstract

Farmed fish are commonly exposed to stress in intensive aquaculture systems, often leading to immune impairment and increased susceptibility to disease. As microbial communities associated with the gut and skin are vital to host health and disease resilience, disruption of microbiome integrity could...

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Published in: Comparative Biochemistry and Physiology Part D: Genomics and Proteomics
ISSN: 1744-117X
Published: Elsevier BV 2021
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URI: https://cronfa.swan.ac.uk/Record/cronfa56111
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As microbial communities associated with the gut and skin are vital to host health and disease resilience, disruption of microbiome integrity could contribute to the adverse consequences of stress exposure. Little is known about how stress affects the fish microbiome, especially during sensitive early life stages when initial colonisation and proliferation of host-associated microbial communities take place. Therefore, we compared the effects of two aquaculture-relevant early-life stressors on the gut and skin microbiome of Atlantic salmon fry (four months post hatching) using 16S rRNA amplicon sequencing. Acute cold stress applied during late embryogenesis had a pronounced, lasting effect on the structure of the skin microbiome, as well as a less consistent effect on the gut microbiome. Follow-up targeted qPCR assays suggested that this is likely due to disruption of the egg shell microbial communities at the initial stages of microbiome colonisation, with persistent effects on community structure. In contrast, chronic post hatching stress altered the structure of the gut microbiome, but not that of the skin. Both types of stress promoted similar Gammaproteobacteria ASVs, particularly within the genera Acinetobacter and Aeromonas, which include several important opportunistic fish pathogens. Our results demonstrate the sensitivity of the salmon microbiome to environmental stressors during early life, with potential associated health impacts on the host. 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spelling 2021-09-22T16:02:39.0823753 v2 56111 2021-01-24 Early life stress causes persistent impacts on the microbiome of Atlantic salmon 3ea91c154926c86f89ea6a761122ecf6 0000-0002-0072-9745 Tamsyn Uren Webster Tamsyn Uren Webster true false 241f2810ab8f56be53ca8af23e384c6e 0000-0003-4403-2509 S Consuegra del Olmo S Consuegra del Olmo true false 1c70acd0fd64edb0856b7cf34393ab02 0000-0003-1650-2729 Carlos Garcia De Leaniz Carlos Garcia De Leaniz true false 2021-01-24 SBI Farmed fish are commonly exposed to stress in intensive aquaculture systems, often leading to immune impairment and increased susceptibility to disease. As microbial communities associated with the gut and skin are vital to host health and disease resilience, disruption of microbiome integrity could contribute to the adverse consequences of stress exposure. Little is known about how stress affects the fish microbiome, especially during sensitive early life stages when initial colonisation and proliferation of host-associated microbial communities take place. Therefore, we compared the effects of two aquaculture-relevant early-life stressors on the gut and skin microbiome of Atlantic salmon fry (four months post hatching) using 16S rRNA amplicon sequencing. Acute cold stress applied during late embryogenesis had a pronounced, lasting effect on the structure of the skin microbiome, as well as a less consistent effect on the gut microbiome. Follow-up targeted qPCR assays suggested that this is likely due to disruption of the egg shell microbial communities at the initial stages of microbiome colonisation, with persistent effects on community structure. In contrast, chronic post hatching stress altered the structure of the gut microbiome, but not that of the skin. Both types of stress promoted similar Gammaproteobacteria ASVs, particularly within the genera Acinetobacter and Aeromonas, which include several important opportunistic fish pathogens. Our results demonstrate the sensitivity of the salmon microbiome to environmental stressors during early life, with potential associated health impacts on the host. We also identified common signatures of stress in the salmon microbiome, which may represent useful microbial stress biomarkers. Journal Article Comparative Biochemistry and Physiology Part D: Genomics and Proteomics 40 100888 Elsevier BV 1744-117X Microbiota; Temperature; Cold shock; Salmo salar; Aquaculture 1 12 2021 2021-12-01 10.1016/j.cbd.2021.100888 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University External research funder(s) paid the OA fee (includes OA grants disbursed by the Library) This work was funded by a BBSRC-NERC, United Kingdom Aqua-culture grant (BB/M026469/1), the Welsh Government and Higher Education Funding Council for Wales (HEFCW) through the Sˆer Cymru National Research Network for Low Carbon Energy and Environment (NRN-LCEE) AQUAWALES project to SC, and the European Regional Development Fund via WEFO and the SMARTAQUA Operation to CGL. 2021-09-22T16:02:39.0823753 2021-01-24T11:43:41.1679165 College of Science Biosciences Tamsyn Uren Webster 0000-0002-0072-9745 1 S Consuegra del Olmo 0000-0003-4403-2509 2 Carlos Garcia De Leaniz 0000-0003-1650-2729 3 56111__20966__9a2f4602697b4e43ac32225ba3453f67.pdf 56111.pdf 2021-09-22T16:01:21.6770973 Output 3820177 application/pdf Version of Record true © 2021 The Authors. This is an open access article under the CC BY license true eng http://creativecommons.org/licenses/by/4.0/
title Early life stress causes persistent impacts on the microbiome of Atlantic salmon
spellingShingle Early life stress causes persistent impacts on the microbiome of Atlantic salmon
Tamsyn Uren Webster
S Consuegra del Olmo
Carlos Garcia De Leaniz
title_short Early life stress causes persistent impacts on the microbiome of Atlantic salmon
title_full Early life stress causes persistent impacts on the microbiome of Atlantic salmon
title_fullStr Early life stress causes persistent impacts on the microbiome of Atlantic salmon
title_full_unstemmed Early life stress causes persistent impacts on the microbiome of Atlantic salmon
title_sort Early life stress causes persistent impacts on the microbiome of Atlantic salmon
author_id_str_mv 3ea91c154926c86f89ea6a761122ecf6
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author_id_fullname_str_mv 3ea91c154926c86f89ea6a761122ecf6_***_Tamsyn Uren Webster
241f2810ab8f56be53ca8af23e384c6e_***_S Consuegra del Olmo
1c70acd0fd64edb0856b7cf34393ab02_***_Carlos Garcia De Leaniz
author Tamsyn Uren Webster
S Consuegra del Olmo
Carlos Garcia De Leaniz
author2 Tamsyn Uren Webster
S Consuegra del Olmo
Carlos Garcia De Leaniz
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description Farmed fish are commonly exposed to stress in intensive aquaculture systems, often leading to immune impairment and increased susceptibility to disease. As microbial communities associated with the gut and skin are vital to host health and disease resilience, disruption of microbiome integrity could contribute to the adverse consequences of stress exposure. Little is known about how stress affects the fish microbiome, especially during sensitive early life stages when initial colonisation and proliferation of host-associated microbial communities take place. Therefore, we compared the effects of two aquaculture-relevant early-life stressors on the gut and skin microbiome of Atlantic salmon fry (four months post hatching) using 16S rRNA amplicon sequencing. Acute cold stress applied during late embryogenesis had a pronounced, lasting effect on the structure of the skin microbiome, as well as a less consistent effect on the gut microbiome. Follow-up targeted qPCR assays suggested that this is likely due to disruption of the egg shell microbial communities at the initial stages of microbiome colonisation, with persistent effects on community structure. In contrast, chronic post hatching stress altered the structure of the gut microbiome, but not that of the skin. Both types of stress promoted similar Gammaproteobacteria ASVs, particularly within the genera Acinetobacter and Aeromonas, which include several important opportunistic fish pathogens. Our results demonstrate the sensitivity of the salmon microbiome to environmental stressors during early life, with potential associated health impacts on the host. We also identified common signatures of stress in the salmon microbiome, which may represent useful microbial stress biomarkers.
published_date 2021-12-01T04:28:58Z
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