Genomic characterization of Volzhskoe tick virus (Bunyaviricetes) from a Hyalomma marginatum tick, Hungary.
Bunyaviricetes
Hyalomma marginatum
Illumina-based viral metagenomic sequencing
Tick
Volzhskoe tick virus
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
15 08 2024
15 08 2024
Historique:
received:
26
06
2024
accepted:
08
08
2024
medline:
16
8
2024
pubmed:
16
8
2024
entrez:
15
8
2024
Statut:
epublish
Résumé
Hyalomma marginatum, a vector for the high-consequence pathogen, the Crimean-Congo hemorrhagic fever virus (CCHFV), needs particular attention due to its impact on public health. Although it is a known vector for CCHFV, its general virome is largely unexplored. Here, we report findings from a citizen science monitoring program aimed to understand the prevalence and diversity of tick-borne pathogens, particularly focusing on Hyalomma ticks in Hungary. In 2021, we identified one adult specimen of Hyalomma marginatum and subjected it to Illumina-based viral metagenomic sequencing. Our analysis revealed sequences of the uncharacterized Volzhskoe tick virus, an unclassified member of the class Bunyaviricetes. The in silico analysis uncovered key genetic regions, including the glycoprotein and the RNA-dependent RNA polymerase (RdRp) coding regions. Phylogenetic analysis indicated a close relationship between our Volzhskoe tick virus sequences and other unclassified Bunyaviricetes species. These related species of unclassified Bunyaviricetes were detected in vastly different geolocations. These findings highlight the remarkable diversity of tick specific viruses and emphasize the need for further research to understand the transmissibility, seroreactivity or the potential pathogenicity of Volzhskoe tick virus and related species.
Identifiants
pubmed: 39147851
doi: 10.1038/s41598-024-69776-8
pii: 10.1038/s41598-024-69776-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
18945Subventions
Organisme : COST
ID : CA21170
Organisme : COST
ID : CA21170
Organisme : COST
ID : CA21170
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : National Research, Development and Innovation Office
ID : RRF-2.3.1-21-2022-00006
Organisme : German Federal Ministry of Education and Research
ID : 13N15449
Organisme : German Federal Ministry of Education and Research
ID : 13N15449
Informations de copyright
© 2024. The Author(s).
Références
Kreuder Johnson, C. et al. Spillover and pandemic properties of zoonotic viruses with high host plasticity. Sci. Rep. 5, 14830. https://doi.org/10.1038/srep14830 (2015).
doi: 10.1038/srep14830
pubmed: 26445169
pmcid: 4595845
Hubalek, Z. & Rudolf, I. Tick-borne viruses in Europe. Parasitol. Res. 111(1), 9–36. https://doi.org/10.1007/s00436-012-2910-1 (2012).
doi: 10.1007/s00436-012-2910-1
pubmed: 22526290
Mora, C. et al. Over half of known human pathogenic diseases can be aggravated by climate change. Nat. Clim. Change 12(9), 869–875. https://doi.org/10.1038/s41558-022-01426-1 (2022).
doi: 10.1038/s41558-022-01426-1
Bente, D. A. et al. Crimean-Congo hemorrhagic fever: History, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antivir. Res. 100(1), 159–189. https://doi.org/10.1016/j.antiviral.2013.07.006 (2013).
doi: 10.1016/j.antiviral.2013.07.006
pubmed: 23906741
Hoogstraal, H. The epidemiology of tick-borne Crimean–Congo hemorrhagic fever in Asia, Europe, and Africa. J. Med. Entomol. 15(4), 307–417. https://doi.org/10.1093/jmedent/15.4.307 (1979).
doi: 10.1093/jmedent/15.4.307
pubmed: 113533
Sparagano, O., George, D., Giangaspero, A. & Spitalska, E. Arthropods and associated arthropod-borne diseases transmitted by migrating birds. The case of ticks and tick-borne pathogens. Vet. Parasitol. 213(1–2), 61–66. https://doi.org/10.1016/j.vetpar.2015.08.028 (2015).
doi: 10.1016/j.vetpar.2015.08.028
pubmed: 26343302
Földvári, G. et al. Ticks and the city: Ectoparasites of the Northern white-breasted hedgehog (Erinaceus roumanicus) in an urban park. Ticks Tick-Borne Dis. 2(4), 231–234. https://doi.org/10.1016/j.ttbdis.2011.09.001 (2011).
doi: 10.1016/j.ttbdis.2011.09.001
pubmed: 22108019
Hornok, S. et al. Synanthropic birds associated with high prevalence of tick-borne rickettsiae and with the first detection of Rickettsia aeschlimannii in Hungary. Vector Borne Zoonotic Dis. 13(2), 77–83. https://doi.org/10.1089/vbz.2012.1032 (2013).
doi: 10.1089/vbz.2012.1032
pubmed: 23289394
Hornok, S. et al. Bird ticks in Hungary reflect western, southern, eastern flyway connections and two genetic lineages of Ixodes frontalis and Haemaphysalis concinna. Parasit. Vectors 9, 101. https://doi.org/10.1186/s13071-016-1365-0 (2016).
doi: 10.1186/s13071-016-1365-0
pubmed: 26912331
pmcid: 4765043
Hornok, S. & Horváth, G. First report of adult Hyalomma marginatum rufipes (vector of Crimean–Congo haemorrhagic fever virus) on cattle under a continental climate in Hungary. Parasit. Vectors 5, 170. https://doi.org/10.1186/1756-3305-5-170 (2012).
doi: 10.1186/1756-3305-5-170
pubmed: 22889105
pmcid: 3436687
Keve, G. et al. Ornithological and molecular evidence of a reproducing Hyalomma rufipes population under continental climate in Europe. Front. Vet. Sci. 10, 1147186. https://doi.org/10.3389/fvets.2023.1147186 (2023).
doi: 10.3389/fvets.2023.1147186
pubmed: 37035818
pmcid: 10073722
Magyar, N. et al. New geographical area on the map of Crimean–Congo hemorrhagic fever virus: First serological evidence in the Hungarian population. Ticks Tick-Borne Dis. 12(1), 101555. https://doi.org/10.1016/j.ttbdis.2020.101555 (2021).
doi: 10.1016/j.ttbdis.2020.101555
pubmed: 33022559
Németh, V. et al. Serologic evidence of Crimean–Congo hemorrhagic fever virus infection in Hungary. Vector Borne Zoonotic Dis. 13(4), 270–272. https://doi.org/10.1089/vbz.2012.1011 (2013).
doi: 10.1089/vbz.2012.1011
pubmed: 23421895
Földes, F. et al. Serologic survey of the Crimean-Congo haemorrhagic fever virus infection among wild rodents in Hungary. Ticks Tick-Borne Dis. 10(6), 101258. https://doi.org/10.1016/j.ttbdis.2019.07.002 (2019).
doi: 10.1016/j.ttbdis.2019.07.002
pubmed: 31302067
Walter, C. T. & Barr, J. N. Recent advances in the molecular and cellular biology of bunyaviruses. J. Gen. Virol. 92(Pt 11), 2467–2484. https://doi.org/10.1099/vir.0.035105-0 (2011).
doi: 10.1099/vir.0.035105-0
pubmed: 21865443
Leventhal, S. S., Wilson, D., Feldmann, H. & Hawman, D. W. A look into bunyavirales genomes: Functions of non-structural (NS) proteins. Viruses https://doi.org/10.3390/v13020314 (2021).
doi: 10.3390/v13020314
pubmed: 33670641
pmcid: 7922539
Patterson, E. I., Villinger, J., Muthoni, J. N., Dobel-Ober, L. & Hughes, G. L. Exploiting insect-specific viruses as a novel strategy to control vector-borne disease. Curr. Opin. Insect. Sci. 39, 50–56. https://doi.org/10.1016/j.cois.2020.02.005 (2020).
doi: 10.1016/j.cois.2020.02.005
pubmed: 32278312
pmcid: 7302987
de Almeida, J. P., Aguiar, E. R., Armache, J. N., Olmo, R. P. & Marques, J. T. The virome of vector mosquitoes. Curr. Opin. Virol. 49, 7–12. https://doi.org/10.1016/j.coviro.2021.04.002 (2021).
doi: 10.1016/j.coviro.2021.04.002
pubmed: 33991759
Olmo, R. P. et al. Mosquito vector competence for dengue is modulated by insect-specific viruses. Nat. Microbiol. 8(1), 135–149. https://doi.org/10.1038/s41564-022-01289-4 (2023).
doi: 10.1038/s41564-022-01289-4
pubmed: 36604511
Földvári, G. et al. Emergence of Hyalomma marginatum and Hyalomma rufipes adults revealed by citizen science tick monitoring in Hungary. Transbound. Emerg. Dis. 69(5), e2240–e2248. https://doi.org/10.1111/tbed.14563 (2022).
doi: 10.1111/tbed.14563
pubmed: 35436033
pmcid: 9790508
Brooks, D. R. & Boeger, W. A. The Stockholm Paradigm: Climate Change and Emerging Disease (University of Chicago Press, 2019).
Muller, R., Poch, O., Delarue, M., Bishop, D. H. & Bouloy, M. Rift Valley fever virus L segment: Correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J. Gen. Virol. 75(Pt 6), 1345–1352. https://doi.org/10.1099/0022-1317-75-6-1345 (1994).
doi: 10.1099/0022-1317-75-6-1345
pubmed: 7515937
Kormelink, R., Garcia, M. L., Goodin, M., Sasaya, T. & Haenni, A. L. Negative-strand RNA viruses: The plant-infecting counterparts. Virus Res. 162(1–2), 184–202. https://doi.org/10.1016/j.virusres.2011.09.028 (2011).
doi: 10.1016/j.virusres.2011.09.028
pubmed: 21963660
Kang, H. J. et al. Evolutionary insights from a genetically divergent hantavirus harbored by the European common mole (Talpa europaea). PLoS ONE 4(7), e6149. https://doi.org/10.1371/journal.pone.0006149 (2009).
doi: 10.1371/journal.pone.0006149
pubmed: 19582155
pmcid: 2702001
Daszak, P., Amuasi, J., Hayman, D., Kuiken, T., Roche, B., Zambrana-Torrelio, C., Buss, P., Dundarova, H., Feferholtz, Y., Földvári, G., Igbinosa, E., Junglen, S., Liu, Q., Suzan, G., Uhart, M., Wannous, C., Woolaston, K., Mosig Reidl, P., O'Brien, K., Pascual, U., Stoett, P., Li, H., Ngo, H. T. (2020). Workshop Report on Biodiversity and Pandemics of the Intergovernmental Platform on Biodiversity and Ecosystem Services. IPBES secretariat, Bonn, Germany. https://doi.org/10.5281/zenodo.4147318
Sameroff, S. et al. Virome of Ixodes ricinus, Dermacentor reticulatus, and Haemaphysalis concinna ticks from Croatia. Viruses https://doi.org/10.3390/v14050929 (2022).
doi: 10.3390/v14050929
pubmed: 35632671
pmcid: 9146755
Tomazatos, A. et al. Discovery and genetic characterization of a novel orthonairovirus in Ixodes ricinus ticks from Danube Delta. Infect. Genet. Evol. 88, 104704. https://doi.org/10.1016/j.meegid.2021.104704 (2021).
doi: 10.1016/j.meegid.2021.104704
pubmed: 33418146
Altamura, L. A. et al. Identification of a novel C-terminal cleavage of Crimean–Congo hemorrhagic fever virus PreGN that leads to generation of an NSM protein. J. Virol. 81(12), 6632–6642. https://doi.org/10.1128/JVI.02730-06 (2007).
doi: 10.1128/JVI.02730-06
pubmed: 17409136
pmcid: 1900101
Bagci, C., Patz, S. & Huson, D. H. DIAMOND+MEGAN: Fast and easy taxonomic and functional analysis of short and long microbiome sequences. Curr. Protoc. 1(3), e59. https://doi.org/10.1002/cpz1.59 (2021).
doi: 10.1002/cpz1.59
pubmed: 33656283
Fernandez-Correa, I. et al. A novel group of avian astroviruses from Neotropical passerine birds broaden the diversity and host range of Astroviridae. Sci. Rep. 9(1), 9513. https://doi.org/10.1038/s41598-019-45889-3 (2019).
doi: 10.1038/s41598-019-45889-3
pubmed: 31266971
pmcid: 6606752
Alex, C. E., Kubiski, S. V., Jackson, K. A., Wack, R. F. & Pesavento, P. A. Amdoparvovirus infections are prevalent, persistent, and genetically diverse in zoo-housed red pandas (Ailurus fulgens). J. Zoo Wildl. Med. 53(1), 83–91. https://doi.org/10.1638/2021-0082 (2022).
doi: 10.1638/2021-0082
pubmed: 35339152
pmcid: 9219412
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25(14), 1754–1760. https://doi.org/10.1093/bioinformatics/btp324 (2009).
doi: 10.1093/bioinformatics/btp324
pubmed: 19451168
pmcid: 2705234
Gasteiger, E. et al. ExPASy: The proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31(13), 3784–3788. https://doi.org/10.1093/nar/gkg563 (2003).
doi: 10.1093/nar/gkg563
pubmed: 12824418
pmcid: 168970
Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32(5), 1792–1797. https://doi.org/10.1093/nar/gkh340 (2004).
doi: 10.1093/nar/gkh340
pubmed: 15034147
pmcid: 390337
Tamura, K., Stecher, G. & Kumar, S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38(7), 3022–3027. https://doi.org/10.1093/molbev/msab120 (2021).
doi: 10.1093/molbev/msab120
pubmed: 33892491
pmcid: 8233496
Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30(9), 1236–1240. https://doi.org/10.1093/bioinformatics/btu031 (2014).
doi: 10.1093/bioinformatics/btu031
pubmed: 24451626
pmcid: 3998142
Bernhofer, M. et al. PredictProtein: Predicting protein structure and function for 29 years. Nucleic Acids Res. 49(W1), W535–W540. https://doi.org/10.1093/nar/gkab354 (2021).
doi: 10.1093/nar/gkab354
pubmed: 33999203
pmcid: 8265159
Steentoft, C. et al. Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J. 32(10), 1478–1488. https://doi.org/10.1038/emboj.2013.79 (2013).
doi: 10.1038/emboj.2013.79
pubmed: 23584533
pmcid: 3655468
Almagro Armenteros, J. J. et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat. Biotechnol. 37(4), 420–423. https://doi.org/10.1038/s41587-019-0036-z (2019).
doi: 10.1038/s41587-019-0036-z
pubmed: 30778233
Duckert, P., Brunak, S. & Blom, N. Prediction of proprotein convertase cleavage sites. Prot. Eng. Des. Sel. 17(1), 107–112. https://doi.org/10.1093/protein/gzh013 (2004).
doi: 10.1093/protein/gzh013
Johnson, L. S., Eddy, S. R. & Portugaly, E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinform. 11, 431. https://doi.org/10.1186/1471-2105-11-431 (2010).
doi: 10.1186/1471-2105-11-431
Hallgren, J., Tsirigos, K. D., Pedersen, M. D., Almagro Armenteros, J. J., Marcatili, P., Nielsen, H., Krogh, A. & Winther, O. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. bioRxiv (2022). https://doi.org/10.1101/2022.04.08.487609
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49(W1), W293–W296. https://doi.org/10.1093/nar/gkab301 (2021).
doi: 10.1093/nar/gkab301
pubmed: 33885785
pmcid: 8265157