The expanding range of emerging tick-borne viruses in Eastern Europe and the Black Sea Region

Koray Ergunay^{1

2

3

4}, Brian P Bourke^{5

6

7}, Drew D Reinbold-Wasson⁸, Mikeljon P Nikolich⁹, Suppaluck P Nelson^{5

6

7}, Laura Caicedo-Quiroga^{5

6

7}, Nataliya Vaydayko¹⁰, Giorgi Kirkitadze⁸, Tamar Chunashvili⁸, Lewis S Long¹¹, Jason K Blackburn¹², Nora G Cleary¹³, Cynthia L Tucker^{5

6}, Yvonne-Marie Linton^{5

6

7}

Affiliations

¹ Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution, 4210 Silver Hill Rd., Suitland, MD, 20746-2863, USA. ergunayk@si.edu.
² One Health Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD, 20910, USA. ergunayk@si.edu.
³ Department of Entomology, Smithsonian Institution-National Museum of Natural History, 10th St NE and Constitution Ave NE, Washington, DC, 20002, USA. ergunayk@si.edu.
⁴ Department of Medical Microbiology, Virology Unit, Faculty of Medicine, Hacettepe University, Ankara, Turkey. ergunayk@si.edu.
⁵ Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution, 4210 Silver Hill Rd., Suitland, MD, 20746-2863, USA.
⁶ One Health Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD, 20910, USA.
⁷ Department of Entomology, Smithsonian Institution-National Museum of Natural History, 10th St NE and Constitution Ave NE, Washington, DC, 20002, USA.
⁸ U.S. Army Medical Research Directorate-Georgia (USAMRD-G), Tbilisi, Georgia.
⁹ Bacterial Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, 20910, USA.
¹⁰ Ukrainian Center of Diseases Control and Monitoring, Kyiv, 04071, Ukraine.
¹¹ Uniformed Services, University of the Health Sciences, Bethesda, MD, 20814, USA.
¹² Emerging Pathogens Institute, University of Florida, Gainesville, FL, 32610, USA.
¹³ One Health Center of Excellence, University of Florida, Gainesville, FL, 32603, USA.

PMID: 37963929
PMCID: PMC10646066
DOI: 10.1038/s41598-023-46879-2

The expanding range of emerging tick-borne viruses in Eastern Europe and the Black Sea Region

Koray Ergunay et al. Sci Rep. 2023.

. 2023 Nov 14;13(1):19824.

doi: 10.1038/s41598-023-46879-2.

Authors

Affiliations

¹ Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution, 4210 Silver Hill Rd., Suitland, MD, 20746-2863, USA. ergunayk@si.edu.
² One Health Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD, 20910, USA. ergunayk@si.edu.
³ Department of Entomology, Smithsonian Institution-National Museum of Natural History, 10th St NE and Constitution Ave NE, Washington, DC, 20002, USA. ergunayk@si.edu.
⁴ Department of Medical Microbiology, Virology Unit, Faculty of Medicine, Hacettepe University, Ankara, Turkey. ergunayk@si.edu.
⁵ Walter Reed Biosystematics Unit, Museum Support Center MRC-534, Smithsonian Institution, 4210 Silver Hill Rd., Suitland, MD, 20746-2863, USA.
⁶ One Health Branch, Walter Reed Army Institute of Research, 503 Robert Grant Ave., Silver Spring, MD, 20910, USA.
⁷ Department of Entomology, Smithsonian Institution-National Museum of Natural History, 10th St NE and Constitution Ave NE, Washington, DC, 20002, USA.
⁸ U.S. Army Medical Research Directorate-Georgia (USAMRD-G), Tbilisi, Georgia.
⁹ Bacterial Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, MD, 20910, USA.
¹⁰ Ukrainian Center of Diseases Control and Monitoring, Kyiv, 04071, Ukraine.
¹¹ Uniformed Services, University of the Health Sciences, Bethesda, MD, 20814, USA.
¹² Emerging Pathogens Institute, University of Florida, Gainesville, FL, 32610, USA.
¹³ One Health Center of Excellence, University of Florida, Gainesville, FL, 32603, USA.

PMID: 37963929
PMCID: PMC10646066
DOI: 10.1038/s41598-023-46879-2

Abstract

We analysed both pooled and individual tick samples collected from four countries in Eastern Europe and the Black Sea region, using metagenome-based nanopore sequencing (NS) and targeted amplification. Initially, 1337 ticks, belonging to 11 species, were screened in 217 pools. Viruses (21 taxa) and human pathogens were detected in 46.5% and 7.3%, respectively. Tick-borne viral pathogens comprised Tacheng Tick Virus 2 (TTV2, 5.9%), Jingmen Tick Virus (JMTV, 0.9%) and Tacheng Tick Virus 1 (TTV1, 0.4%). An association of tick species with individual virus taxa was observed, with the exception of TTV2, which was observed in both Dermacentor and Haemaphysalis species. Individual ticks from pools with pathogen detection were then further screened by targeted amplification and then NS, which provided extensive genome data and revealed probable pathogen Haseki Tick Virus (HTV, 10.2%). Two distinct TTV2 clades were observed in phylogenetic analysis, one of which included closely related Dermacentor reticulatus Uukuviruses. JMTV detection indicated integrated virus sequences. Overall, we observed an expansion of newly documented pathogenic tick-borne viruses into Europe, with TTV1 being identified on the continent for the first time. These viruses should be included in the diagnostic assessment of symptomatic cases associated with tick bites and vector surveillance efforts. NS is shown as a useful tool for monitoring tick-associated pathogens in pooled or individual samples.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The funders of the research had no influence on results presented. The opinions or assertions contained herein are the private views of the authors, and are not to be construed as official, or as reflecting true views of the Department of the Army, Navy or the Department of Defense. Material contained within this publication has been reviewed by the Walter Reed Army Institute of Research. There is no objection to its presentation and / or publication.

Figures

**Figure 1**
The maximum likelihood consensus tree of the phenuivirus polymerase sequences (783 amino acids), constructed using 1000 replicates. Branches achieving ≥ 95% bootstrap support are annotated with red dots. Tacheng Tick Virus 2 (TTV2) lineages are marked. Viruses are indicated by GenBank accession, name and isolate identifier where available. Sequences detected in the study are indicated by sample IDs.

**Figure 2**
The maximum likelihood consensus tree of the nairovirus polymerase (A: 335 amino acids, B: 359 amino acids), glycoprotein precursor (C: 115 amino acids) and nucleocapsid (D: 135 amino acids) sequences. The trees are constructed using 1000 replicates. Branches achieving ≥ 95% bootstrap support are annotated with red dots. Tacheng Tick Virus 1 (TTV1) sequences in each alignment are marked. Viruses are indicated by GenBank accession, name and isolate identifier where available. Sequences detected in the study are indicated by sample IDs.

**Figure 3**
Map indicating the tick sampling locations in the study. Sites with detectable human pathogens are marked by a triangle.

See this image and copyright information in PMC

References

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The expanding range of emerging tick-borne viruses in Eastern Europe and the Black Sea Region

Affiliations

The expanding range of emerging tick-borne viruses in Eastern Europe and the Black Sea Region

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

LinkOut - more resources

Full Text Sources

Miscellaneous