Novel clades of tick-borne pathogenic nairoviruses in Europe

Koray Ergunay; Brian P Bourke; Drew D Reinbold-Wasson; Laura Caicedo-Quiroga; Nataliya Vaydayko; Giorgi Kirkitadze; Tamar Chunashvili; Cynthia L Tucker; Yvonne-Marie Linton

doi:10.1016/j.meegid.2024.105593

Novel clades of tick-borne pathogenic nairoviruses in Europe

Infect Genet Evol. 2024 Apr 16:121:105593. doi: 10.1016/j.meegid.2024.105593. Online ahead of print.

Authors

Koray Ergunay¹, Brian P Bourke², Drew D Reinbold-Wasson³, Laura Caicedo-Quiroga², Nataliya Vaydayko³, Giorgi Kirkitadze³, Tamar Chunashvili³, Cynthia L Tucker⁴, Yvonne-Marie Linton²

Affiliations

¹ Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution, 4210 Silver Hill Rd., Suitland, MD 20746, USA; One Health Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD 20910, USA; Department of Entomology, Smithsonian Institution - National Museum of Natural History, 10th St NE & Constitution Ave NE, Washington, DC 20002, USA; Department of Medical Microbiology, Virology Unit, Faculty of Medicine, Hacettepe University, Ankara, Turkey. Electronic address: ergunayk@si.edu.
² Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution, 4210 Silver Hill Rd., Suitland, MD 20746, USA; One Health Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD 20910, USA; Department of Entomology, Smithsonian Institution - National Museum of Natural History, 10th St NE & Constitution Ave NE, Washington, DC 20002, USA.
³ Walter Reed Army Institute of Research - Europe - Middle East, Tbilisi, Georgia.
⁴ Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution, 4210 Silver Hill Rd., Suitland, MD 20746, USA; One Health Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD 20910, USA.

PMID: 38636618
DOI: 10.1016/j.meegid.2024.105593

Abstract

Members of the Orthonairovirus genus (family Nairoviridae) include many tick-borne viruses of significant human and animal health impact, with several recently-documented pathogenic viruses lacking sufficient epidemiological information. We screened 215 adult ticks of seven species collected in Bulgaria, Georgia, Latvia and Poland for orthonairoviruses, followed by nanopore sequencing (NS) for genome characterization. Initial generic amplification revealed Sulina virus (SULV, Orthonairovirus sulinaense), for which an updated amplification assay was used, revealing an overall prevalence of 2.7% in Ixodes ricinus ticks from Latvia. Three complete and additional partial SULV genomes were generated, that consistently formed a separate, distinct clade with further intragroup divergence in the maximum likelihood analyses. Comparisons with previously described viruses from Romania exhibited similar genome topologies, albeit with divergent motifs and cleavage sites on the glycoprotein precursor. Preliminary evidence of recombination involving the S segment was documented, in addition to variations in predicted viral glycoproteins. Generic screening further identified Tacheng tick virus 1 (TCTV1, Orthonairovirus tachengense), with documented human infections, in Dermacentor reticulatus ticks from Poland, with a prevalence of 0.9%. Subsequent NS and assembly provided the first complete TCTV1 genome outside of China, where it was originally described. Phylogenetic analysis of virus genome segments revealed TCTV1-Poland as a discrete taxon within the TCTV1 cluster in the Orthonairovirus genus, representing a geographically segregated clade. Comparable genome topology with TCTV1 from China was observed, aside from minor variations in the M segment. Similar to SULV, TCTV1 exhibited several mismatches on previously described screening primer binding sites, likely to prevent amplification. These findings indicate presence of novel TCTV1 and SULV clades in Eastern Europe, confirming the expansion of orthonairoviruses with pathogenic potential.

Keywords: Clade; Metagenome; Nairovirus; Tick.