Wild salmon pathogens discovered that could pose a threat to aquaculture

Researchers from the University of British Columbia and Fisheries and Oceans Canada have identified three new viruses that are impacting populations of endangered salmon in the North Pacific. They used DNA sequencing and virus-specific tests to screen more than 6,000 dead and dying salmon in the wild, in hatcheries and on fish farms. Sampling from three different cohorts allowed the researchers to determine the distribution of the virus.

Three new viruses – including one type that has never previously infected fish – have been identified in populations of both wild and farmed salmon off the coast of British Columbia, Canada.

Two of the viruses were found in wild, hatchery and cultured salmon. One virus was found in farmed adult salmon. This finding is notable because it suggests that the viruses are distributed differently among the Chinook and sockeye salmon populations. It also suggests that the virus has a different route of transmission within and between populations of farmed, wild and hatchery salmon.

"We found the new viruses widely distributed in dead and dying farmed salmon and in wild salmon," UBC virologist Curtis Suttle told phys.org. "It emphasises the potential role that viral disease may play in the population dynamics of wild fish stocks, and the threat that these viruses may pose to aquaculture."

Populations of sockeye and Chinook salmon have been declining for the past 30 years. A potential contributor to their decline could be viral infection. These populations of salmon play a critical role in Canada’s Pacific ecosystem, making their conservation a long-term goal and high priority. The species have supported the Indigenous population for thousands of years and are a key element of Canada’s aquaculture strategy.

Pacific salmon species have supported coastal ecosystems and Indigenous populations surrounding the North Pacific Ocean for tens of millennia. Today, through their anadromous life history, salmon continue to transport nutrients between aquatic and terrestrial environments, supply the primary food sources for orca whales and sea lions and provide economic livelihoods for local communities. In the Northeast Pacific, widespread declines of Chinook and sockeye salmon have occurred in the last 30 years, leading some populations to the brink of extirpation , and a cause of great concern to Indigenous groups, commercial and recreational fishers, and the general public. Although the exact number of salmon spawning in rivers is unknown, there are large declines in sockeye salmon over a large geographic area. Similarly, Chinook salmon stocks are at only a small percentage of their historic levels, and more than 50 stocks are extinct.

It is thought that infectious disease may contribute to salmon declines, but little is known about infectious agents, especially viruses, endemic to Pacific salmon. Infectious disease has been identified as a potential factor in poor early marine survival in migratory salmon; an immune response to viruses has been associated with mortality in wild migratory smolts and adults, and in unspecified mortalities of salmon in marine net pens in British Columbia (BC). For instance, immune responses to viruses such as Infectious haematopoietic necrosis virus (IHNV) and potentially undiscovered viruses, have been associated with mortality in wild juvenile salmon. This is an important observation as mortality of juvenile salmon can be as high as ~90% transitioning from fresh water to the marine environment. Together, these suggest that there are undiscovered viruses which may contribute to decreased survival of Pacific salmon but a concerted effort to look for viruses that may contribute to mortality has been absent.

Here, virus-discovery was implemented to screen for viruses associated with mortality. Together, sequencing of dead or moribund aquaculture salmon and live-sampled wild salmon, in-situ hybridization, and epidemiological surveys revealed that previously unknown viruses, some of which are associated with disease, infect wild salmon from different populations.

Three evolutionarily divergent groups viruses Arenaviridae , Nidovirales, Reoviridae that can be highly pathogenic. Arenaviruses were relatively common and geographically widespread in migratory juvenile Chinook and sockeye salmon in the marine environment . Whereas, the nidovirus was spatially localised and predominantly observed at high prevalence over multiple years in Chinook salmon leaving freshwater hatcheries. Finally, the reovirus was detected only in farmed Chinook salmon

The distribution and abundance of the different viruses varied markedly. Arenaviruses were relatively common and geographically widespread in migratory juvenile Chinook and sockeye salmon in the marine environment. Whereas, the nidovirus was spatially localised and predominantly observed at high prevalence over multiple years in Chinook salmon leaving freshwater hatcheries. Finally, the reovirus was detected only in farmed Chinook salmon .

With the exception of their relatively recent discovery in snakesand frogfish, arenaviruses were thought to solely infect mammals. The arenaviruses reported here share less than 15% amino-acid sequence similarity (in the RdRp) to those from mammals and snakes, and define a new monophyletic evolutionary group, the pescarenaviruses. The absence of clear sequence homology in the glycoprotein, the difference in genome segmentation, as well as phylogenetic analysis of the replicase demonstrate that pescarenaviruses share a common but ancient ancestor with arenaviruses infecting snakes and mammals. We recommend these fish-infecting arenaviruses are assigned to the new genus Pescarenavirus, with those infecting Chinook and sockeye salmon being assigned to the species Salmon pescarenavirus (SPAV), respectively.

Farmed Chinook salmon positive for SPAV-1 displayed pathology and symptoms consistent with disease including inflammation of the spleen and liver, as well as tubule necrosis and hyperplasia in the kidney. Clinically, salmon presented with yellow fluid on the pyloric caeca and swim bladder, pale gills with haemorrhaging on the surface, and anaemia. Wild Chinook and sockeye that tested positive for arenavirus infection, but which were clinically healthy when sampled, showed few histological lesions. In-situ hybridization revealed that arenaviruses were concentrated mainly in macrophage-like cells, melanomacrophages, red-blood cells (RBCs) and endotheliocytes. 

These findings are consistent with localisation of arenaviruses in mammals and snakes, although in contrast to snakes and fish, mammalian red blood cells are not nucleated so the similarity likely only extends to nucleated cells. SPAV-1 and −2 shared similar cell tropism within Chinook and sockeye salmon, respectively. In one out of the eight Chinook samples examined, moderate chronic-active hepatitis was reported, and staining for SPAV-1 was identified in the area affected by inflammation, while in the other samples SPAV-1 was confined to reticuloendothelial cells in the liver tissue or in the sinusoids. More lesions were observed in dead farmed Chinook, where disease progression is more advanced. Our observations indicate that arenaviruses are replicating in red-blood cells, and occur in the macrophages and leukocytes that consume the infected cells. Moreover, the observed pathological changes in arenavirus-infected fish, including anaemia, and lesions in the gills, kidney and liver would be expected for viruses that infect red-blood cells. These results are the first empirical evidence for arenavirus infection in fish, and suggest that SPAV, like many other arenaviruses, has the potential to be a causative agent of disease.

Viral disease is a potential threat to wild fish stocks; yet little is known about viruses circulating in wild, farmed, or hatchery salmon. Here, through metatranscriptomic surveys, we reveal several previously unknown viruses that were discovered in dead and dying aquaculture fish, and show them to also occur in wild and hatchery-reared fish. Depending on the viral and host species, the viruses range from being localised to widespread, from infecting <1% to >20% of fish, and being from within the limits of detection to very high loads. Our results are consistent with some of these viruses being causative agents of disease, making it critical to understand their possible roles in salmon mortality and the decline of wild salmon populations, and their potential interactions with net-pen fish farming and hatchery rearing. Viral discovery in moribund individuals followed by extensive surveillance and histopathological localisation are powerful tools towards the ultimate goals of identifying causative agents of disease and understanding the impact of infectious agents in wild populations. These insights are crucial as juvenile salmon that are in less than optimal health are expected to have lower rates of survival in the wild. Continued surveillance and knowledge of endemic and emerging virus infections in these iconic salmon species is beneficial for their conservation.