Host Jump of an Exotic Fish Rhabdovirus into a New Class of Animals Poses a Disease Threat to Amphibians

Author:

Emmenegger Eveline J.1ORCID,Bueren Emma K.12,Conway Carla M.1ORCID,Sanders George E.3,Hendrix A. Noble45,Schroeder Tamara6,Di Cicco Emiliano7,Pham Phuc H.8,Lumsden John S.8,Clouthier Sharon C.6ORCID

Affiliation:

1. U.S. Geological Survey, Western Fisheries Research Center (WFRC), 6505 NE 65th Street, Seattle, WA 98115, USA

2. Department of Biology, Indiana University, 1001 E 3rd St, Bloomington, IN 47405, USA

3. Department of Comparative Medicine, University of Washington, Seattle, WA 98195, USA

4. QEDA Consulting, 4007 Densmore Avenue N, Seattle, WA 98103, USA

5. School of Aquatic and Fishery Sciences, University of Washington, Seattle, WA 98195, USA

6. Freshwater Institute, Fisheries and Oceans Canada (DFO), 501 University Crescent, Winnipeg, MB R3T 2N6, Canada

7. Pacific Salmon Foundation (PSF), 1682 W 7th Ave., Vancouver, BC V6J 4S6, Canada

8. Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada

Abstract

Spring viremia of carp virus (SVCV) is a rhabdovirus that primarily infects cyprinid finfishes and causes a disease notifiable to the World Organization for Animal Health. Amphibians, which are sympatric with cyprinids in freshwater ecosystems, are considered non-permissive hosts of rhabdoviruses. The potential host range expansion of SVCV in an atypical host species was evaluated by testing the susceptibility of amphibians native to the Pacific Northwest. Larval long-toed salamanders Ambystoma macrodactylum and Pacific tree frog Pseudacris regilla tadpoles were exposed to SVCV strains from genotypes Ia, Ib, Ic, or Id by either intraperitoneal injection, immersion, or cohabitation with virus-infected koi Cyprinus rubrofuscus. Cumulative mortality was 100% for salamanders injected with SVCV, 98–100% for tadpoles exposed to virus via immersion, and 0–100% for tadpoles cohabited with SVCV-infected koi. Many of the animals that died exhibited clinical signs of disease and SVCV RNA was found by in situ hybridization in tissue sections of immersion-exposed tadpoles, particularly in the cells of the gastrointestinal tract and liver. SVCV was also detected by plaque assay and RT-qPCR testing in both amphibian species regardless of the virus exposure method, and viable virus was detected up to 28 days after initial exposure. Recovery of infectious virus from naïve tadpoles cohabited with SVCV-infected koi further demonstrated that SVCV transmission can occur between classes of ectothermic vertebrates. Collectively, these results indicated that SVCV, a fish rhabdovirus, can be transmitted to and cause lethal disease in two amphibian species. Therefore, members of all five of the major vertebrate groups (mammals, birds, reptiles, fish, and amphibians) appear to be vulnerable to rhabdovirus infections. Future research studying potential spillover and spillback infections of aquatic rhabdoviruses between foreign and domestic amphibian and fish species will provide insights into the stressors driving novel interclass virus transmission events.

Funder

U.S. Geological Survey—USGS

Publisher

MDPI AG

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