Cyclic Hypoxia Exposure Accelerates the Progression of Amoebic Gill Disease

Tina Oldham,Philip Crosbie,Tim Dempster,Mark Adams,Barbara Nowak

doi:10.3390/pathogens9080597

Tina Oldham, Philip Crosbie + Show 3 more

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https://doi.org/10.3390/pathogens9080597

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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.

Highlights

Limiting dissolved oxygen (DO) conditions, termed hypoxic, occur in Atlantic salmon (Salmo salar) cages around the world, and are predicted to increase in frequency and severity as the global climate warms [1,2,3,4]
We examine if cyclic exposure to moderate hypoxia, similar to conditions documented in marine aquaculture cages, alters Amoebic gill disease (AGD) acquisition, progression, and prognosis in post-smolt Atlantic salmon
N. perurans were detected on the gills of individuals in both the normoxic and hypoxic treatments at all three sample collection periods

Summary

Introduction

Limiting dissolved oxygen (DO) conditions, termed hypoxic, occur in Atlantic salmon (Salmo salar) cages around the world, and are predicted to increase in frequency and severity as the global climate warms [1,2,3,4]. In the wild, limited evidence suggests that salmon avoid areas with low DO [5]. In marine cages during the seawater grow-out phase of production, the response of salmon to low DO is variable. In several other marine cage studies, salmon remained in moderately hypoxic waters at levels known to reduce feed intake, growth, and immune competence, despite other areas of the cage having higher DO [3,6,7].

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