Cyclic Hypoxia Exposure Accelerates the Progression of Amoebic Gill Disease

Abstract

Amoebic gill disease (AGD), caused by the amoeba Neoparamoeba perurans, has led to considerable economic losses in every major Atlantic salmon producing country, and is increasing in frequency. The most serious infections occur during summer and autumn, when temperatures are high and poor dissolved oxygen (DO) conditions are most common. Here, we tested if exposure to cyclic hypoxia at DO saturations of 40–60% altered the course of infection with N. perurans compared to normoxic controls maintained at ≥90% DO saturation. Although hypoxia exposure did not increase initial susceptibility to N. perurans, it accelerated progression of the disease. By 7 days post-inoculation, amoeba counts estimated from qPCR analysis were 1.7 times higher in the hypoxic treatment than in normoxic controls, and cumulative mortalities were twice as high (16 ± 4% and 8 ± 2%), respectively. At 10 days post-inoculation, however, there were no differences between amoeba counts in the hypoxic and normoxic treatments, nor in the percentage of filaments with AGD lesions (control = 74 ± 2.8%, hypoxic = 69 ± 3.3%), or number of lamellae per lesion (control = 30 ± 0.9%, hypoxic = 27.9 ± 0.9%) as determined by histological examination. Cumulative mortalities at the termination of the experiment were similarly high in both treatments (hypoxic = 60 ± 2%, normoxic = 53 ± 11%). These results reveal that exposure to cyclic hypoxia in a diel pattern, equivalent to what salmon are exposed to in marine aquaculture cages, accelerated the progression of AGD in post-smolts.

Experimental exposure to low concentrations of Neoparamoebaperurans induces amoebic gill disease in Atlantic salmon

“…In the current experiment, the gill samples were positive for N. perurans later than in challenges where higher concentrations of amoebae were applied (Benedicenti et al 2015;Collins et al 2017;Oldham et al 2020). There was a high variability in the severity of AGD lesions both within and between individuals and the variable size of lesions within the second left gill arch suggested that the lesions were induced at different time points or that there was high individual variability in host response to the amoeba.…”

“…2017; Oldham et al. 2020). There was a high variability in the severity of AGD lesions both within and between individuals and the variable size of lesions within the second left gill arch suggested that the lesions were induced at different time points or that there was high individual variability in host response to the amoeba.…”

Development of Atlantic Salmon (Salmo salar L.) Under Hypoxic Conditions Induced Sustained Changes in Expression of Immune Genes and Reduced Resistance to Moritella viscosa

“…The immune system and protection against pathogens are among the main concerns. Comparisons of disease resistance in Atlantic salmon kept at normal and low levels of DO produced different results, such as absence of effect in challenge with salmon alphavirus ( Andersen et al, 2010) and accelerated progression of amoebic gill disease (Oldham et al, 2020). To our knowledge, remote effects of hypoxia on the immune system and protection against pathogens in Atlantic salmon have not been reported until present.…”

“…For example, hypoxia appeared not to differentially affect the severity of pancreas disease in salmon infected with salmonid alphavirus (Andersen et al, 2010). On the other hand, in Atlantic salmon post-smolts infected with amoebe Neoparamoeba perurans (the agent of amoebic gill disease), cyclic hypoxia accelerated the progression of the disease and increased amoeba counts and mortality (Oldham et al, 2020). Niklasson et al (2011) showed that low DO levels affected the mucosal immune system of the intestine, through downregulations of nuclear factor kappa B, and differential expression of interleukins in combination with higher temperature.…”

Host Response of Atlantic Salmon (Salmo salar) Re-Inoculated with Paramoeba perurans

“…The frequency of infection recurrence, which may necessitate multiple freshwater immersion treatments within one life cycle in the industry setting, will contribute to an elevated stress response in the fish. The resultant increase in plasma cortisol has been shown to suppress immunity, which can contribute to increased fish susceptibility and further exacerbate the issue of re-infection [ 34 , 35 ]. This work attempts to try and elucidate the response of fish re-inoculated P. perurans and to determine whether an adaptive response is initiated.…”