Emergence of Viral hemorrhagic septicemia virus in the North American Great Lakes region is ­associated with low viral genetic diversity

Abstract

Viral hemorrhagic septicemia virus (VHSV) is a fish rhabdovirus that causes disease in a broad range of marine and freshwater hosts. The known geographic range includes the Northern Atlantic and Pacific Oceans, and recently it has invaded the Great Lakes region of North Ame rica. The goal of this work was to characterize genetic diversity of Great Lakes VHSV isolates at the early stage of this viral emergence by comparing a partial glycoprotein (G) gene sequence (669 nt) of 108 isolates collected from 2003 to 2009 from 31 species and at 37 sites. Phylogenetic analysis showed that all isolates fell into sub-lineage IVb within the major VHSV genetic group IV. Among these 108 isolates, genetic diversity was low, with a maximum of 1.05% within the 669 nt region. There were 11 unique sequences, designated vcG001 to vcG011. Two dominant sequence types, vcG001 and vcG002, accounted for 90% (97 of 108) of the isolates. The vcG001 isolates were most widespread. We saw no apparent association of sequence type with host or year of isolation, but we did note a spatial pattern, in which vcG002 isolates were more prevalent in the easternmost sub-regions, including inland New York state and the St. Lawrence Seaway. Different sequence types were found among isolates from single disease outbreaks, and mixtures of types were evident within 2 isolates from individual fish. Overall, the genetic diversity of VHSV in the Great Lakes region was found to be extremely low, consistent with an introduction of a new virus into a geographic region with previously naïve host populations. KEY WORDS: Emerging infectious diseases · Fish disease · Fish rhabdovirus · Genotyping · Molecular epidemiology · Phylogenetic analysis · Viral haemorrhagic septicaemia virus · Viral hemorrhagic septicemia virus · VHSV Resale or republication not permitted without written consent of the publisherDis Aquat Org 96: [29][30][31][32][33][34][35][36][37][38][39][40][41][42][43] 2011 the 1950s (Wolf 1988, Smail 2000, Skall et al. 2005. Because outbreaks of VHSV are associated with acute systemic disease, hemorrhage, and mortality rates that can mount up to 90% in a broad range of susceptible species, VHSV is listed by the World Organization for Animal Health (formerly the Office International des Epizooties, still referred to as OIE) as one of only 9 reportable fish diseases (OIE 2010). In 1988, VHSV was first detected on the Pacific coast of North America (Meyers & Winton 1995). Subsequent surveys revealed an extensive reservoir of VHSV in wild marine fish of the northeast Pacific Ocean, and VHS epidemics have been reported in wild Pacific herring and sardines (Meyers & Winton 1995, Hedrick et al. 2003. VHSV has also been isolated from wild and farmed olive flounder Paralichthys olivaceus in Japan and Korea (Nishizawa et al. 2002, Kim et al. 2003. Subsequent surveys in European waters also found an extensive VHSV reservoir involving many marine fish species (Skall et al. 2005). Therefore, prior to its recent emergence in the Great Lakes, VHSV was con...

Molecular epidemiology of viral haemorrhagic septicaemia virus (VHSV) in British Columbia, Canada, reveals transmission from wild to farmed fish

“…The simplest hypothesis for this close association of sequence types within an outbreak is that mutations arise during viral replication in a fish and are subsequently introduced and established into other fish associated with the mortality event. Observation of genetic heterogeneity of sequences obtained from single fish as observed in our study and others (Einer-Jensen et al 2004, Thompson et al 2011) support the notion of VHSV quasispecies within a single host. In contrast to the presence of sequence types differing by only 1 or 2 bases, it was also revealed in the dataset presented herein that VHSV outbreaks could be defined by sequence types differing in as much as 24 bases (i.e.…”

“…However, the VHSV population structure within BC is in contrast to that observed for VHSV emerging in the Great Lakes. Within the BC data set, the ephemeral appearance of 42 sequence types over the 19 yr collection period reveals the occurrence of ongoing sequence divergence and lack of a predominant sequence type, while in the Great Lakes, 2 dominant sequence types accounted for 90% of the isolates collected over a 6 yr period (Thompson et al 2011). The higher abundance of viral variants observed among the BC data set in comparison to the Great Lakes isolates is likely reflective of the temporal differences in viral presence between the 2 regions.…”

Virulence of viral hemorrhagic septicemia virus (VHSV) genotypes Ia, IVa, IVb, and IVc in five fish species

“…In the other 2 experimental treatments, which were rainbow trout/high injection challenge dose and Pacific herring/low immersion challenge dose, geno- Thompson et al 2011, Ito et al 2012, Pierce & Stepien 2012. Therefore, the observation that genotype IVc caused significantly lower mortality than IVb in the Great Lakes yellow perch provides a preliminary indication that the emergence of genotype IVb may have been associated with an adaptation to higher virulence in yellow perch.…”

European freshwater VHSV genotype Ia isolates divide into two distinct subpopulations

“…Genotype Ie isolates have been obtained from both the freshwater and the marine environment in Georgia and Turkey (Nishizawa et al 2006). Genotype IV isolates, from North America and Asia (Skall et al 2005), are divided into the sublineages IVa and IVb, of which IVa is primarily restricted to the marine environment in both North America and Asia (Meyers & Winton 1995, Nishizawa et al 2002, Kim et al 2003, Hedrick et al 2003, Lee et al 2007), whereas sublineage IVb isolates have been observed in both freshwater and marine systems in North America only (Gagné et al 2007, Kane-Sutton et al 2010, Thompson et al 2011.…”