Comparison of Endemic and Epidemic Vesicular Stomatitis Virus Lineages in Culicoides sonorensis Midges

Abstract

Vesicular stomatitis virus (VSV) primarily infects livestock and is transmitted by direct contact and vectored by Culicoides midges (Diptera: Ceratopogonidae). Endemic to Central and South America, specific VSV lineages spread northward out of endemic regions of Mexico and into the U.S. sporadically every five to ten years. In 2012, a monophyletic epidemic lineage 1.1 successfully spread northward into the U.S. In contrast, the closest endemic ancestor, lineage 1.2, remained circulating exclusively in endemic regions in Mexico. It is not clear what roles virus-animal interactions and/or virus-vector interactions play in the ability of specific viral lineages to escape endemic regions in Mexico and successfully cause outbreaks in the U.S., nor the genetic basis for such incursions. Whole-genome sequencing of epidemic VSV 1.1 and endemic VSV 1.2 revealed significant differences in just seven amino acids. Previous studies in swine showed that VSV 1.1 was more virulent than VSV 1.2. Here, we compared the efficiency of these two viral lineages to infect the vector Culicoides sonorensis (Wirth and Jones) and disseminate to salivary glands for subsequent transmission. Our results showed that midges orally infected with the epidemic VSV 1.1 lineage had significantly higher infection dissemination rates compared to those infected with the endemic VSV 1.2 lineage. Thus, in addition to affecting virus-animal interactions, as seen with higher virulence in pigs, small genetic changes may also affect virus-vector interactions, contributing to the ability of specific viral lineages to escape endemic regions via vector-borne transmission.

Culicoides-Specific Fitness Increase of Vesicular Stomatitis Virus in Insect-to-Insect Infections

“…Three VSV-New Jersey (VSV-NJ) virus strains were used for midge infections; one laboratory-adapted positive control strain and two more recent outbreak isolates [30]. Strain 82-34333 is a Colorado bovine isolate from the 1982 epizootic outbreak [22] that has been passed numerous times in both mammalian and insect cells.…”

“…Strain rNJ0806VCB is a synthesized bovine isolate from a 2006 enzootic outbreak in Vera Cruz, Mexico [31]. Both synthesized strains were produced in BHK-21 cells [30] and are courtesy of S. Pauszek and L. Rodriguez, Plum Island Animal Disease Center, NY [31]. Virus strains were passaged one time at an MOI of 0.1 in porcine skin fibroblast cells (mammalian-derived VSV) and in Culicoides cells (insect-derived VSV) to produce high titer viral stocks that were stored at −80 • C for subsequent midge infections.…”

“…The field isolate viral stocks rNJ0806VCB and rNJ0612NME6 (originally produced in BHK-21 cells) were replicated once in each of our test host cell sources (porcine and Culicoides) [30]. The laboratory stock isolate, 82-34333, had undergone multiple passages in multiple species of cell lines over 30 years.…”

Vesicular stomatitis Indiana virus near-full-length genome sequences reveal low genetic diversity during the 2019 outbreak in Colorado, USA

“…The virus periodically causes outbreaks in central and northern Mexico, and spreads into the US, causing outbreaks in the US on an approximately 5–8 year cycle ( 7 , 9 , 10 ). Recent studies indicate that epidemic lineages of VSNJV present different phenotypes than endemic lineages in both vertebrate and invertebrate hosts ( 11 , 12 ). Epidemic lineages causing outbreaks in the US likely originate in endemic regions of Mexico and spread northward ( 7 , 9 ).…”