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Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch)

There is tremendous variation in life-history strategies among anadromous salmonids. Species that enter the ocean environment at small sizes (< 20 g) are likely under more physiological pressure from pathogens; however, little data is available on responses at these early stages. With this in min...

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Autores principales: Braden, Laura M., Michaud, Dylan, Groman, David, Byrne, Phil, Hori, Tiago S., Fast, Mark D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272145/
https://www.ncbi.nlm.nih.gov/pubmed/37322246
http://dx.doi.org/10.1038/s41598-023-36632-0
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author Braden, Laura M.
Michaud, Dylan
Groman, David
Byrne, Phil
Hori, Tiago S.
Fast, Mark D.
author_facet Braden, Laura M.
Michaud, Dylan
Groman, David
Byrne, Phil
Hori, Tiago S.
Fast, Mark D.
author_sort Braden, Laura M.
collection PubMed
description There is tremendous variation in life-history strategies among anadromous salmonids. Species that enter the ocean environment at small sizes (< 20 g) are likely under more physiological pressure from pathogens; however, little data is available on responses at these early stages. With this in mind, we performed salmon louse challenges with Coho salmon either immediately after seawater entry (SW; ca. 10 g) or after 30 days in SW (ca. 20 g). Irrespective of size or time in SW, parasites were rapidly rejected by the host, with > 90% of all parasites lost by 16 days post-infection (dpi). Rejection was concomitant with host epithelial granulomatous infiltrations that initially targeted the embedded frontal filament (4 dpi) and the entire parasite by 10 dpi. Illumina sequencing, followed by functional enrichment analysis, revealed a concerted defense response in the fin within 1 dpi that included multiple innate and adaptive immunity components. Strikingly, early indications of an allergic-type inflammatory response were associated with chitin sensing pathways orchestrated by early overexpression of the IgE-receptor, fcer1g. Additionally, there was profound overexpression of several classes of c-type lectin receptors, including dectin-2, mincle, and dc-sign at 1 dpi onward. These profiles and upregulation of cellular effector markers were corroborated by histopathological evaluation, revealing the simultaneous presence of mast cell/eosinophilic granular cells, sacciform cells, macrophages/histiocytes, and granulocytes in fin. At 10 dpi and concurrent with parasite expulsion, there was evidence of immunoregulation in addition to tissue remodelling pathways. At 16 dpi, the response was effectively abrogated. Simultaneous profiling of the parasite transcriptome revealed early induction of chitin metabolism and immunomodulation, toxin production and ECM degradation; however, after 7 dpi, these were replaced with overexpression of stress and immune defense genes. These data present the first evidence for Coho salmon demonstrating chitin- and sugar moiety-sensing as key drivers of salmon louse rejection.
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spelling pubmed-102721452023-06-17 Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch) Braden, Laura M. Michaud, Dylan Groman, David Byrne, Phil Hori, Tiago S. Fast, Mark D. Sci Rep Article There is tremendous variation in life-history strategies among anadromous salmonids. Species that enter the ocean environment at small sizes (< 20 g) are likely under more physiological pressure from pathogens; however, little data is available on responses at these early stages. With this in mind, we performed salmon louse challenges with Coho salmon either immediately after seawater entry (SW; ca. 10 g) or after 30 days in SW (ca. 20 g). Irrespective of size or time in SW, parasites were rapidly rejected by the host, with > 90% of all parasites lost by 16 days post-infection (dpi). Rejection was concomitant with host epithelial granulomatous infiltrations that initially targeted the embedded frontal filament (4 dpi) and the entire parasite by 10 dpi. Illumina sequencing, followed by functional enrichment analysis, revealed a concerted defense response in the fin within 1 dpi that included multiple innate and adaptive immunity components. Strikingly, early indications of an allergic-type inflammatory response were associated with chitin sensing pathways orchestrated by early overexpression of the IgE-receptor, fcer1g. Additionally, there was profound overexpression of several classes of c-type lectin receptors, including dectin-2, mincle, and dc-sign at 1 dpi onward. These profiles and upregulation of cellular effector markers were corroborated by histopathological evaluation, revealing the simultaneous presence of mast cell/eosinophilic granular cells, sacciform cells, macrophages/histiocytes, and granulocytes in fin. At 10 dpi and concurrent with parasite expulsion, there was evidence of immunoregulation in addition to tissue remodelling pathways. At 16 dpi, the response was effectively abrogated. Simultaneous profiling of the parasite transcriptome revealed early induction of chitin metabolism and immunomodulation, toxin production and ECM degradation; however, after 7 dpi, these were replaced with overexpression of stress and immune defense genes. These data present the first evidence for Coho salmon demonstrating chitin- and sugar moiety-sensing as key drivers of salmon louse rejection. Nature Publishing Group UK 2023-06-15 /pmc/articles/PMC10272145/ /pubmed/37322246 http://dx.doi.org/10.1038/s41598-023-36632-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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 Article
Braden, Laura M.
Michaud, Dylan
Groman, David
Byrne, Phil
Hori, Tiago S.
Fast, Mark D.
Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch)
title Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch)
title_full Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch)
title_fullStr Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch)
title_full_unstemmed Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch)
title_short Rejection of Lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in Coho salmon (Oncorhynchus kisutch)
title_sort rejection of lepeophtheirus salmonis driven in part by chitin sensing is not impacted by seawater acclimitization in coho salmon (oncorhynchus kisutch)
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272145/
https://www.ncbi.nlm.nih.gov/pubmed/37322246
http://dx.doi.org/10.1038/s41598-023-36632-0
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