Virome Analysis of Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis Ticks Reveals Novel Highly Divergent Vertebrate and Invertebrate Viruses

Abstract

A wide range of bacterial pathogens have been identified in ticks, yet the diversity of viruses in ticks is largely unexplored. In the United States, Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis are among the principal tick species associated with pathogen transmission. We used high-throughput sequencing to characterize the viromes of these tick species and identified the presence of Powassan virus and eight novel viruses. These included the most divergent nairovirus described to date, two new clades of tick-borne phleboviruses, a mononegavirus, and viruses with similarity to plant and insect viruses. Our analysis revealed that ticks are reservoirs for a wide range of viruses and suggests that discovery and characterization of tickborne viruses will have implications for viral taxonomy and may provide insight into tick-transmitted diseases. IMPORTANCETicks are implicated as vectors of a wide array of human and animal pathogens. To better understand the extent of tick-borne diseases, it is crucial to uncover the full range of microbial agents associated with ticks. Our current knowledge of the diversity of tick-associated viruses is limited, in part due to the lack of investigation of tick viromes. In this study, we examined the viromes of three tick species from the United States. We found that ticks are hosts to highly divergent viruses across several taxa, including ones previously associated with human disease. Our data underscore the diversity of tick-associated viruses and provide the foundation for further studies into viral etiology of tick-borne diseases.

Expansion of the Metazoan Virosphere: Progress, Pitfalls, and Prospects

“…It has 'filled in' shallower parts of the tree, finding close relatives of iconic human pathogens, such as new influenzas in toads and eels (Shi et al 2018). It has also discovered new deep branches, such as clades of insectinfecting Partitiviruses (Webster et al 2015;Shi et al 2016a) and Luteo/Sobemo-like viruses (Tokarz et al 2014;Shi et al 2016a), and whole new families, such as the Chuviruses (Li et al 2015). This in turn has led to renewed interest in inferring deep viral phylogenies (Koonin et al 2015;Shi et al 2016a), and has prompted proposals for large-scale updates of higher-level virus taxonomy (Aiewsakun and Simmonds 2018).…”

“…It has provided a better perspective on host-association and switching (Geoghegan et al 2017;Dolja and Koonin 2018;Shi et al 2018), found familiar virus lineages with unexpected genome sizes and structures (Li et al 2015;Shi et al 2016a;Shi et al 2016b), and uncovered an unexpectedly dynamic history of 'modular' protein swapping (Koonin et al 2015;Shi et al 2016a). Finally, merely having a PCR product from a metagenomic sample can provide an experimental route to the functional biology of an uncultured virus (van Mierlo et al 2014).…”

Emerging Horizons for Tick-Borne Pathogens: From the ‘One Pathogen–one Disease’ Vision to the Pathobiome Paradigm

“…In the USA, a similar study, undertaken by Lipkin et al, characterized the virome of different tick species. Powassan virus, a well-known human pathogenic tick-borne virus, and eight novel viruses belonging to nairovirus, phlebovirus and mononegavirus genera were identified among the three ticks assessed [53]. New viruses recently identified in ticks by NGS are listed in Table 2.…”

“…Ixodes scapularis [53] Blacklegged tick Phlebovirus (BTPV) Unknown Ixodes scapularis [53] American dog tick Phlebovirus (ADTPV) Unknown Ixodes scapularis/D. variabilis [53] Monongavirales-like virus Unknown Ixodes scapularis [53] Phlebovirus (Hearltand virus) Severe febrile illness Amblyomma americanum [84] Shibuinji virus (New tick-borne virus phlebovirus)…”

“…variabilis [53] Monongavirales-like virus Unknown Ixodes scapularis [53] Phlebovirus (Hearltand virus) Severe febrile illness Amblyomma americanum [84] Shibuinji virus (New tick-borne virus phlebovirus)…”