Host–pathogen interaction unveiled by immune, oxidative stress, and cytokine expression analysis to experimental Saprolegnia parasitica infection in Nile tilapia

Abstract

The present study evaluated the pathogenicity, immunological, and oxidant/antioxidant responses against Saprolegnia parasitica (S. parasitica) infection in Nile tilapia (Oreochromis niloticus). Three groups of Nile tilapia were assigned as the control group (no zoospores exposure). The other two groups were challenged by Saprolegnia zoospores; one was used for sampling, and the other for mortality monitoring. The study lasted 3 weeks and was sampled at three point times at 1, 2, and 3 weeks. Results showed that S. parasitica zoospores were pathogenic to Nile tilapia, causing a cumulative mortality rate of 86.6%. Immunoglobulin M and C- reactive protein (IgM and CRP) levels showed a similar trend being significantly (P < 0.05, P < 0.001) higher in the infected group at weeks 1, 2, and 3, respectively, compared to the control group. Oxidant and antioxidant parameters in gills revealed that Malondialdehyde (MDA) level was significantly higher in the infected group compared to the control group. While catalase, glutathione peroxidase, and superoxide dismutase (CAT, GSH, and SOD) levels were significantly decreased in the infected group compared to the control group. Compared to the control, the tumor necrosis factor-α (TNF-α) gene was firmly upregulated in gill tissue at all-time points, particularly at day 14 post-infection. Meanwhile, Interleukin 1-β (IL-1 β) gene was significantly upregulated only at days 7 and 14 post-infection compared to control. Histopathological examination revealed destructive and degenerative changes in both skin and gills of experimentally infected Nile tilapia. Our findings suggest that Nile tilapia-S. parasitica infection model was successful in better understanding of pathogenicity and host (fish)-pathogen (oomycete) interactions, where the induced oxidative stress and upregulation of particular immune biomarkers in response to S. parasitica infection may play a crucial role in fish defense against oomycetes in fish.

The First Report on Saprolegnia parasitica and Neoparamoeba perurans Isolated from Atlantic Salmon (Salmo salar) Reared in Korea

“…This report is consistent with the symptoms observed in the histopathological analysis of the gill covers and abdominal muscles (Figure 5B,C) in this study, which included necrosis, hemorrhage, and inflammatory cell infiltration. S. parasitica possesses various virulence factors that act on the host's extracellular effectors (proteases, gluconases, and hydrolases), simultaneously attacking host cells and tissues while being secreted into the host's extracellular space, ultimately leading to alteration in the structure and function of cells [63]. Furthermore, it is stated that by secreting proteins (glycoside hydrolases) that aid in the breakdown of cell walls into the extracellular space, S. parasitica infiltrates the host's tissues, leading to epidermal destruction and respiratory failure due to osmotic imbalance resulting from the degeneration of secondary lamellae, ultimately resulting in morality [63][64][65].…”