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

Abstract

There is tremendous variation in life-history strategies among anadromous salmonids. Species that enter the ocean environment at small sizes (<&#x2009;20&#xa0;g) are likely under more physiological pressure from pathogens; however, little data is available on responses at these early stages.&#xa0;With this in mind, we performed salmon louse challenges with Coho salmon either immediately after seawater entry (SW; ca. 10&#xa0;g) or after 30&#xa0;days in SW (ca. 20&#xa0;g). Irrespective of size or time in SW, parasites were rapidly rejected by the host, with&#x2009;>&#x2009;90% of all parasites lost by 16&#xa0;days post-infection (dpi). Rejection was concomitant&#xa0;with host epithelial granulomatous infiltrations that initially targeted the embedded frontal filament (4&#xa0;dpi) and the entire parasite by 10&#xa0;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,&#xa0;fcer1g. Additionally, there was profound overexpression of several classes of c-type lectin receptors, including&#xa0;dectin-2,&#xa0;mincle, and&#xa0;dc-sign&#xa0;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&#xa0;dpi and concurrent with parasite expulsion, there was evidence of immunoregulation in addition to tissue remodelling pathways. At 16&#xa0;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&#xa0;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.