Characterization of vertically and cross-species transmitted viruses in the cestode parasiteSchistocephalus solidus

Abstract

13Parasitic flatworms (Neodermata) represent a public health and economic burden due to associated 14 debilitating diseases and limited therapeutic treatments available. Despite their importance, there 15 is scarce information regarding flatworm-associated microbes. We report the discovery of six RNA 16 viruses in the cestode Schistocephalus solidus. None were closely related to classified viruses and 17 they represent new taxa. Mining transcriptomic data revealed the broad distribution of these 18 viruses in Alaskan and European S. solidus populations. We demonstrate through in vitro culture 19 of S. solidus that five of these viruses are vertically transmitted. With experimental infections and 20 field-sampling, we show that one of the viruses is transmitted to parasitized hosts. The impact of 21 these viruses in parasite fitness and pathogenicity, and in host-parasite co-evolutionary dynamics 22 remains to be determined. The detection of six novel viruses in this first characterization of viruses 23 in Neodermatans likely represents a fraction of virus diversity in parasitic flatworms. 24 25 26 29Trematodes, commonly known as flukes, and cestodes, known as tapeworms, are of particular 30 interest because around 25-30% of humans alone are currently infected with at least one of these 31 worm species. Several of the pathologies associated with these parasite infections are considered 32 major neglected diseases as they affect countries in the Americas, Asia, and Africa (1). The most 33 notorious example is Schistosomiasis, caused by diverse species of Schistosomes and considered 34 the second most deadly parasitic disease after malaria (2). The blood fluke Schistosoma 35 haematobium and the liver flukes Opisthorchis viverrini and Clonorchis sinensis are recognized 36 as group I carcinogens by the International Agency for Research on Cancer (3-5). Fascioliasis, 37 caused by infection with trematodes from the genus Fasciola upon ingestion of contaminated water 38 plants, has detrimental impacts in humans and economically important livestock including pigs, 39 cattle, and sheep (6-8). The most well-known cestodes are Taenia spp., Echinococcus spp., and 40 Hymenolepis nana. Infections with cestodes are chronic, can remain asymptomatic for long 41 periods, and symptoms are often misdiagnosed, making these diseases difficult to target and treat. 42 Serious effects of parasite infection include cysticercosis and seizures due to Taenia solium, cysts 43 or tumors that grow in the liver, lungs, and other organs with Echinococcosis infection, and 44 weakness, headaches, anorexia, abdominal pain, and diarrhea associated with Hymenolepiasis (9-45 11). Fisheries and, in particular, aquaculture are also largely impacted by parasitic infections due 46 to the high prevalence and densities of worms in fishes that serve as either intermediate or 47 definitive hosts (12). 48 Despite their high prevalence and negative impacts, diseases associated with parasitic flatworm 49 infections are difficult to prevent or treat. The main metho...