Characterizing the virome of Ixodes ricinus ticks from northern Europe

Abstract

RNA viruses are abundant infectious agents and present in all domains of life. Arthropods, including ticks, are well known as vectors of many viruses of concern for human and animal health. Despite their obvious importance, the extent and structure of viral diversity in ticks is still poorly understood, particularly in Europe. Using a bulk RNA-sequencing approach that captures the complete transcriptome, we analysed the virome of the most common tick in Europe – Ixodes ricinus. In total, RNA sequencing was performed on six libraries consisting of 33 I. ricinus nymphs and adults sampled in Norway. Despite the small number of animals surveyed, our virus identification pipeline revealed nine diverse and novel viral species, phylogenetically positioned within four different viral groups – bunyaviruses, luteoviruses, mononegavirales and partitiviruses – and sometimes characterized by extensive genetic diversity including a potentially novel genus of bunyaviruses. This work sheds new light on the virus diversity in I. ricinus, expands our knowledge of potential host/vector-associations and tick-transmitted viruses within several viral groups, and pushes the latitudinal limit where it is likely to find tick-associated viruses. Notably, our phylogenetic analysis revealed the presence of tick-specific virus clades that span multiple continents, highlighting the role of ticks as important virus reservoirs.

Extensive Diversity of RNA Viruses in Australian Ticks

“…The most closely related viruses are also tick-associated and were isolated from ticks in Norway and North America (Fig. 6) (14, 33). Timbillica tick Phenui-like virus 1 grouped more closely with viruses found to infect ticks of the Ixodes genus rather than with Albatross Island virus (previously known as Hunter Island virus) identified in avian ticks collected from albatross in Tasmania (21).…”

“…A number of studies have used bacterial 16S rRNA-based metagenomics, as well as PCR and immunoassay-based methods, to search for known or novel tick-associated bacterial pathogens that may be present in Australian ticks (11-13). Additional studies have used more powerful, bulk RNA sequencing-based metagenomic approaches to identify viruses in diverse tick populations, although not those from Australia (14). Although ticks carry a diverse virome and are associated with the transmission of viral pathogens in parts of Europe, North America, Asia, and Africa (15-19), there has been no comprehensive metagenomic study of the virome of ticks in Australia.…”

“…We have recently shown that meta-transcriptomics (i.e. bulk shotgun RNA-sequencing) is a powerful tool for the discovery of novel viruses and other microbial pathogens from both host and tick-derived samples (14, 23-25). Importantly, because total RNA is sequenced, meta-transcriptomics provides information on the total “infectome” of the sample and can be used to the identify viruses, bacteria, fungi, and other eukaryotes present within a sample (26).…”

Meta-transcriptomic comparison of the RNA viromes of the mosquito vectors Culex pipiens and Culex torrentium in northern Europe

“…The mitochondrial COX1 gene, mined from the sequence data, and all contigs with RdRp-motifs was mapped back, using Bowtie2 (31), against all quality trimmed libraries to estimate abundance. A virus was considered to be in high abundance if: (i) it represented >0.1% of total non-ribosomal RNA in the library, and (ii) if the abundance was higher to that of abundant host COX1 gene (12, 32), and hence likely to be mosquito associated. Hits that were below the level of cross-library contamination due to index-hopping, measured as 0.1% of the most abundant library for the respective virus species or less than 1 read per million mapped to a specific virus contig, was considered negative (coloured grey in Table 1 and Table 2, respectively).…”

Identification of new viruses specific to the honey bee mite Varroa destructor

“…Members of this group have a similar genomic structure with two ORFs spanning 3 to 4.2 kb. This group includes viruses and viral sequences described in other acarine species like the deer tick (Ixodes scapularis) and the American dog tick (Dermacentor variabilis) (Harvey et al 2019;Levin et al 2016;Levin et al 2019;Pettersson et al 2017;Sadeghi et al 2018;Shi et al 2016;Webster et al 2016) and not much information about their incidence and replication in a specific host has been reported. Nevertheless, given the mentioned similarities and the replicative activity of these viruses (see below), these V. destructor associated viruses could define a new family of +ssRNA viruses infecting invertebrates.…”