Hypoxia tolerance and responses to hypoxic stress during heart and skeletal muscle inflammation in Atlantic salmon (Salmo salar).

Morten Lund,Marta Alarcon,Gerrit Timmerhaus,Mark Powell,Vidar Aspehaug,Maria Krudtaa Dahle,Espen Rimstad,Sven Martin Jørgensen

doi:10.1371/journal.pone.0181109

Abstract

Heart and skeletal muscle inflammation (HSMI) is associated with Piscine orthoreovirus (PRV) infection and is an important disease in Atlantic salmon (Salmo salar) aquaculture. Since PRV infects erythrocytes and farmed salmon frequently experience environmental hypoxia, the current study examined mutual effects of PRV infection and hypoxia on pathogenesis and fish performance. Furthermore, effects of HSMI on hypoxia tolerance, cardiorespiratory performance and blood oxygen transport were studied. A cohabitation trial including PRV-infected post-smolts exposed to periodic hypoxic stress (4 h of 40% O2; PRV-H) at 4, 7 and 10 weeks post-infection (WPI) and infected fish reared under normoxic conditions (PRV) was conducted. Periodic hypoxic stress did not influence infection levels or histopathological changes in the heart. Individual incipient lethal oxygen saturation (ILOS) was examined using a standardized hypoxia challenge test (HCT). At 7 WPI, i.e. peak level of infection, both PRV and PRV-H groups exhibited reduced hypoxia tolerance compared to non-infected fish. Three weeks later (10 WPI), during peak levels of pathological changes, reduced hypoxia tolerance was still observed for the PRV group while PRV-H performed equal to non-infected fish, implying a positive effect of the repeated exposure to hypoxic stress. This was in line with maximum heart rate (fHmax) measurements, showing equal performance of PRV-H and non-infected groups, but lower fHmax above 19°C as well as lower temperature optimum (Topt) for aerobic scope for PRV, suggesting reduced cardiac performance and thermal tolerance. In contrast, the PRV-H group had reduced hemoglobin-oxygen affinity compared to non-infected fish. In conclusion, Atlantic salmon suffering from HSMI have reduced hypoxia tolerance and cardiac performance, which can be improved by preconditioning fish to transient hypoxic stress episodes.

Highlights

Heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar) is an important viral disease in Norwegian aquaculture [1,2]
There were no significant differences in body weight or condition factor between infected groups (PRV versus Piscine orthoreovirus (PRV)-H group) at any time-points
Body weight of PRV and PRV-H fish included in the hypoxia challenge test (HCT) was significantly higher compared to the Ctrl group at 4 weeks post-infection (WPI) but not at the later time-points (S3 Fig)

Summary

Introduction

Heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar) is an important viral disease in Norwegian aquaculture [1,2]. Piscine orthoreovirus (PRV) is associated with HSMI [6] and has been detected in farmed salmonids in Ireland, Chile, Japan and Canada [7,8,9,10,11,12,13] and in wild salmonids [14]. One may hypothesize that the viral processing and immune responses may affect hemoglobin production and oxygen binding and transport capacity of infected erythrocytes. This may have consequences for the hypoxia- and stress-tolerance of infected fish. Apart from some studies showing reduced cardiac performance to infectious cardiomyopathies in fish [24,25,26], more knowledge is needed with regards to the secondary cardiorespiratory effects of viral infections, and in particular PRV infection which targets both erythrocytes and cardiac muscle in salmonids

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