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Evolution of a group of tick-associated iflaviruses

Evolution of a group of tick-associated iflaviruses
The multiple micro-organisms, parasites or viruses, associated with ticks represent "influential passengers" that can impact the vertebrate hosts on which the ticks perform their blood meals, but also the ticks themselves. We focused on a group of RNA viruses frequently associated with arthropods, and more recently discovered in ticks, the iflaviruses. Through a scan of transcriptomic assemblies from 27 different tick species, we identified nine complete genomic sequences attributed to the iflavirus family, in Ixodes ricinus and then in four other tick species, representing five novel viral species in total. Our phylogenetic analysis demonstrates the absence of strict coevolution between iflaviruses and ticks, and implies several changes in tick host species during the evolution of these viruses. The remaining unknown is the effect of these viruses on the reproductive success of ticks.

Context and issues

Ticks are at the centre of a complex web of interactions, including many microorganisms, parasites and viruses, which can be pathogenic to the animal and human hosts on which ticks take their blood meal. But the impact of these "influential passengers" on the biology and fitness of the ticks themselves must also be explored to better understand the system. Here we focused on a particular group of RNA viruses, the iflaviruses, which are already known in many arthropods of multiple orders, where they often have a pathogenic effect on their invertebrate host. Recently, iflaviruses have also been detected in an increasing number of tick species, but very little was known about this group in terms of evolutionary patterns and distribution in ticks, both inter- and intra-specific.

Results

A complete iflavirus genome sequence was first identified in a brain transcriptome of Ixodes ricinus, by chance. This led us to scan a large number of transcriptome assembly data for both I. ricinus and other tick species, 27 species in all. We were able to identify nine genomic sequences of this virus, including several in I. ricinus. In I. ricinus, the virus is present in several European populations (Switzerland, North-East and North-West France), but its prevalence remains low. In all, we identified five different species, associated respectively with I. ricinus, I. frontalis, I. holocyclus, I. vespertilionis, and Hyalomma dromedarii. We then showed by phylogenetic analysis that these species do not evolve in parallel with their hosts, suggesting multiple host tick change events and probably an absence of vertical transmission between ticks. We also demonstrated that an iflavirus sequence identified in a cell line of Ixodes scapularis (line ISE6), an American tick species, is almost identical to sequences found in Ixodes ricinus, which can only be explained by contamination between biological materials.

Perspectives

The perspectives of this work will be to continue to explore the transcriptome data to identify new sequences of this group, which would allow us to refine the study of their evolution, and to attempt to evaluate the impact of these viruses on the fitness of ticks, particularly in I. ricinus.

Valorisation

A publication relating this work has been produced, in the journal Archives of Virology.

Bibliographic references

Romain Daveu, Caroline Hervet, Louane Sigrist, Davide Sassera, Aaron Jex, Karine Labadie, Jean-Marc Aury, Olivier Plantard, Claude Rispe (2021). Sequence diversity and evolution of a group of iflaviruses associated with ticks. Archives of Virology, 166 (7), 1843-1852, https://dx.doi.org/10.1007/s00705-021-05060-8, https://hal.inrae.fr/hal-03272097