Differential vector competence of Ornithodoros soft ticks for African swine fever virus: What if it involves more than just crossing organic barriers in ticks?

Rémi Pereira De Oliveira,Maxime Duhayon,Laurence Vial,Adalberto A Pérez De León,Renaud Lancelot,Evelyne Hutet,Marie-Frédérique Le Potier,Fernando Boinas,Serhii Filatov,Frédéric Paboeuf

doi:10.1186/s13071-020-04497-1

Abstract

BackgroundSeveral species of soft ticks in genus Ornithodoros are known vectors and reservoirs of African swine fever virus (ASFV). However, the underlying mechanisms of vector competence for ASFV across Ornithodoros species remain to be fully understood. To that end, this study compared ASFV replication and dissemination as well as virus vertical transmission to descendants between Ornithodorosmoubata, O. erraticus, and O. verrucosus in relation to what is known about the ability of these soft tick species to transmit ASFV to pigs. To mimic the natural situation, a more realistic model was used where soft ticks were exposed to ASFV by allowing them to engorge on viremic pigs.MethodsOrnithodoros moubata ticks were infected with the ASFV strains Liv13/33 (genotype I) or Georgia2007/1 (genotype II), O. erraticus with OurT88/1 (genotype I) or Georgia2007/1 (genotype II), and O. verrucosus with Ukr12/Zapo (genotype II), resulting in five different tick–virus pairs. Quantitative PCR (qPCR) assays targeting the VP72 ASFV gene was carried out over several months on crushed ticks to study viral replication kinetics. Viral titration assays were also carried out on crushed ticks 2 months post infection to confirm virus survival in soft ticks. Ticks were dissected. and DNA was individually extracted from the following organs to study ASFV dissemination: intestine, salivary glands, and reproductive organs. DNA extracts from each organ were tested by qPCR. Lastly, larval or first nymph-stage progeny emerging from hatching eggs were tested by qPCR to assess ASFV vertical transmission.ResultsComparative analyses revealed higher rates of ASFV replication and dissemination in O. moubata infected with Liv13/33, while the opposite was observed for O. erraticus infected with Georgia2007/1 and for O. verrucosus with Ukr12/Zapo. Intermediate profiles were found for O. moubata infected with Georgia2007/1 and for O. erraticus with OurT88/1. Vertical transmission occurred efficiently in O. moubata infected with Liv13/33, and at very low rates in O. erraticus infected with OurT88/1.ConclusionsThis study provides molecular data indicating that viral replication and dissemination in Ornithodoros ticks are major mechanisms underlying ASFV horizontal and vertical transmission. However, our results indicate that other determinants beyond viral replication also influence ASFV vector competence. Further research is required to fully understand this process in soft ticks.Graphical

Highlights

Several species of soft ticks in genus Ornithodoros are known vectors and reservoirs of African swine fever virus (ASFV)
The other two ASFV strains belong to genotype I: the Liv13/33 strain isolated in 1983 from O. moubata inhabiting warthog burrows in Zambia [23], and the OurT88/1 strain isolated in 1988 from O. erraticus collected from pig facilities in Portugal [5]
Mortality in ASFV infected ticks The tick–virus pairs O. moubata–Liv13/33 (OmL) and O. moubata–Georgia2007/1 (OmG) showed very high mortality rates (100 and 73%, respectively), while those of O. erraticus–Georgia2007/1 (OeG), O. erraticus–OurT88/1 (OeO), and O. verrucosus–Ukr12/Zapo (OvZ) survived to ASFV infection and showed mortality rates of < 5% (2.8, 2.1, and 0%, respectively)

Summary

Introduction

Several species of soft ticks in genus Ornithodoros are known vectors and reservoirs of African swine fever virus (ASFV). In parts of Africa where ASFV is endemic, soft tick vectors enable the persistence of virus transmission within a sylvatic cycle involving warthogs, and occasionally serve as a source of infection for reemergence of the disease in domestic pigs [3]. Quarantine, herd depopulation, and zoning are the only options to eradicate ASF outbreaks and prevent their spread because an efficient vaccine to control ASF remains to be developed [13] This situation highlights the need to assess the vector competence (including virus reservoir role) of soft ticks established in parts of the world where ASFV is currently present or classified as a high-consequence foreign animal disease with the potential to be introduced [14]

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Results

Conclusion