Impacts of jellyfish homogenates on Atlantic salmon (Salmo salar) gill and head kidney cells

Abstract

Gill pathology in farmed Atlantic salmon has become one of the most serious causes of mortality and economic loss. A growing concern in some regions of the industry are jellyfish blooms which have been linked to mortality events. Cytotoxic effects of jellyfish nematocysts/toxins have been described, however, our understanding of impacts of jellyfish ‘stings’ in salmon is limited. Development of in vitro and in vivo models could help elucidate the impacts jellyfish have on salmon and potential contributions to chronic gill pathologies. Jellyfish (Cyanea capillata; Aurelia aurita; Phacellophora camtschatica) were collected from multiple sites and nematocyst homogenates were generated to assess their impacts on Atlantic salmon kidney in vitro and gill cells in vivo. Homogenates contained over 90 identified proteins, characterized by numerous enzymes, structural proteins, toxin precursors, signaling molecules (JNK, ERK, p38), and calcium ion modulators. Filter-sterilized homogenates caused rapid and extensive cytopathic effects in Atlantic Salmon Kidney cells in vitro. This toxicity was (1) dose dependent, (2) consistent across freeze-thaws, and (3) media/cells from treated cultures did not replicate cytopathic effect in new Atlantic Salmon Kidney cell monolayers. A descriptive analysis of histological changes in the gill indicated no major morphologic changes noted in gills, however, consistent minor changes were observed in both the gill arch epithelium and the gill filaments. The greatest impacts following HJN flush were within 3 h and a significant shift between these exposures at 24 h driven by increased expression of healing, redox and inflammatory genes (plekfh1a, mmp13, xrc33, gpx2, timp2-d and gsta) in the unfiltered vs the filter-sterilized nematocyst homogenate samples.