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Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon

BACKGROUND: Rapidly spreading parasitic infections like amoebic gill disease (AGD) are increasingly problematic for Atlantic salmon reared in aquaculture facilities and potentially pose a risk to wild fish species in surrounding waters. Currently, it is not known whether susceptibility to AGD differ...

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Autores principales: Schaal, Patrick, Cheaib, Bachar, Kaufmann, Joshka, Phillips, Karl, Ryder, Liz, McGinnity, Phil, Llewellyn, Martin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9479442/
https://www.ncbi.nlm.nih.gov/pubmed/36109797
http://dx.doi.org/10.1186/s42523-022-00203-x
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author Schaal, Patrick
Cheaib, Bachar
Kaufmann, Joshka
Phillips, Karl
Ryder, Liz
McGinnity, Phil
Llewellyn, Martin
author_facet Schaal, Patrick
Cheaib, Bachar
Kaufmann, Joshka
Phillips, Karl
Ryder, Liz
McGinnity, Phil
Llewellyn, Martin
author_sort Schaal, Patrick
collection PubMed
description BACKGROUND: Rapidly spreading parasitic infections like amoebic gill disease (AGD) are increasingly problematic for Atlantic salmon reared in aquaculture facilities and potentially pose a risk to wild fish species in surrounding waters. Currently, it is not known whether susceptibility to AGD differs between wild and farmed salmon. Wild Atlantic salmon populations are declining and this emerging disease could represent an additional threat to their long-term viability. A better understanding of how AGD affects fish health is therefore relevant for the accurate assessment of the associated risk, both to farming and to the well-being of wild populations. In this study, we assessed the impact of natural exposure to AGD on wild, hybrid and farmed post-smolt Atlantic salmon reared in a sea farm together under common garden conditions. RESULTS: Wild fish showed substantially higher mortality levels (64%) than farmed fish (25%), with intermediate levels for hybrid fish (39%) suggesting that AGD susceptibility has an additive genetic basis. Metabolic rate measures representing physiological performance were similar among the genetic groups but were significantly lower in AGD-symptomatic fish than healthy fish. Gut microbial diversity was significantly lower in infected fish. We observed major shifts in gut microbial community composition in response to AGD infections. In symptomatic fish the relative abundance of key taxa Aliivibrio, Marinomonas and Pseudoalteromonas declined, whereas the abundance of Polaribacter and Vibrio increased compared to healthy fish. CONCLUSIONS: Our results highlight the stress AGD imposes on fish physiology and suggest that low metabolic-rate fish phenotypes may be associated with better infection outcomes. We consider the role increased AGD outbreak events and a warmer future may have in driving secondary bacterial infections and in reducing performance in farmed and wild fish. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00203-x.
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spelling pubmed-94794422022-09-17 Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon Schaal, Patrick Cheaib, Bachar Kaufmann, Joshka Phillips, Karl Ryder, Liz McGinnity, Phil Llewellyn, Martin Anim Microbiome Research BACKGROUND: Rapidly spreading parasitic infections like amoebic gill disease (AGD) are increasingly problematic for Atlantic salmon reared in aquaculture facilities and potentially pose a risk to wild fish species in surrounding waters. Currently, it is not known whether susceptibility to AGD differs between wild and farmed salmon. Wild Atlantic salmon populations are declining and this emerging disease could represent an additional threat to their long-term viability. A better understanding of how AGD affects fish health is therefore relevant for the accurate assessment of the associated risk, both to farming and to the well-being of wild populations. In this study, we assessed the impact of natural exposure to AGD on wild, hybrid and farmed post-smolt Atlantic salmon reared in a sea farm together under common garden conditions. RESULTS: Wild fish showed substantially higher mortality levels (64%) than farmed fish (25%), with intermediate levels for hybrid fish (39%) suggesting that AGD susceptibility has an additive genetic basis. Metabolic rate measures representing physiological performance were similar among the genetic groups but were significantly lower in AGD-symptomatic fish than healthy fish. Gut microbial diversity was significantly lower in infected fish. We observed major shifts in gut microbial community composition in response to AGD infections. In symptomatic fish the relative abundance of key taxa Aliivibrio, Marinomonas and Pseudoalteromonas declined, whereas the abundance of Polaribacter and Vibrio increased compared to healthy fish. CONCLUSIONS: Our results highlight the stress AGD imposes on fish physiology and suggest that low metabolic-rate fish phenotypes may be associated with better infection outcomes. We consider the role increased AGD outbreak events and a warmer future may have in driving secondary bacterial infections and in reducing performance in farmed and wild fish. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00203-x. BioMed Central 2022-09-15 /pmc/articles/PMC9479442/ /pubmed/36109797 http://dx.doi.org/10.1186/s42523-022-00203-x Text en © The Author(s) 2022 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/) .
spellingShingle Research
Schaal, Patrick
Cheaib, Bachar
Kaufmann, Joshka
Phillips, Karl
Ryder, Liz
McGinnity, Phil
Llewellyn, Martin
Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon
title Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon
title_full Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon
title_fullStr Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon
title_full_unstemmed Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon
title_short Links between host genetics, metabolism, gut microbiome and amoebic gill disease (AGD) in Atlantic salmon
title_sort links between host genetics, metabolism, gut microbiome and amoebic gill disease (agd) in atlantic salmon
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9479442/
https://www.ncbi.nlm.nih.gov/pubmed/36109797
http://dx.doi.org/10.1186/s42523-022-00203-x
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