Phylogenetic relationships of a rabies virus isolate in Costa Rica
DOI:
https://doi.org/10.22458/urj.v14i1.3713Keywords:
phylogenetic analysis, Next-generation Sequencing (NGS), lineage, Desmodus rotundus, Costa RicaAbstract
Introduction: The sylvatic cycle of rabies is a significant sanitary burden in Central America. The Costa Rican government monitors cases since 1985 and infections from bats are still reported for wild animals, livestock, and humans, generating a need of further pathogen characterization in the region. Objective: To compare rabies phylogenetic analyses from complete genomes with nucleoprotein gene studies. Methods: For the phylogenetic analyses we used four rabies tissue samples collected in 2018, and generated complete genomes by Next-Generation sequencing (NGS). We also extracted RNA from tissues of confirmed cases and generated ssDNA using several primers. Double-stranded DNA was generated and used to generate genomic libraries. Results: We describe, for the first-time, the complete genome of four sequences of the rabies virus isolated in Costa Rica in 2018. Complete genome trees resembled the topology of nucleoprotein gene trees. All isolates were related to Desmodus rotundus. One sample group into Lineage (L)2, and the remaining samples group in L1, matched previous reports from regional rabies viruses. Conclusion: Our method produces valid viral assemblies from clinical specimens without target enrichment or viral isolation.
References
Almeida, M. F., Martorelli, L. F. A., Aires, C. C., Sallum, P. C., Durigon, E. L., & Massad, E. (2005). Experimental rabies infection in haematophagous bats Desmodus rotundus. Epidemiology and Infection, 133(3), 523–527. https://doi.org/10.1017/S0950268804003656
Amarilla, A. C. F., Pompei, J. C. A., Araujo, D. B., Vázquez, F. A., Galeano, R. R., Delgado, L. M., Bogado, G., Colman, M., Sanabria, L., Iamamoto, K., Garcia, R., Assis, D., Recalde, R., Martorelli, L. F., Quiñones, E., Cabello, A., Martini, M., Cosivi, O., Durigon, E. L., & Favoretto, S. R. (2018). Re-emergence of rabies virus maintained by canid populations in Paraguay. Zoonoses and Public Health, 65(1), 222–226. https://doi.org/10.1111/zph.12392
Badilla, X., Pérez-Herra, V., Quirós, L., Morice, A., Jiménez, E., Sáenz, E., Salazar, F., Fernández, R., Orciari, L., Yager, P., Whitfield, S., & Rupprecht, C. E. (2003). Human rabies: A reemerging disease in Costa Rica? Emerging Infectious Diseases, 9(6), 721–723. https://doi.org/10.3201/eid0906.020632
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. V., Vyahhi, N., Tesler, G., Alekseyev, M. A., & Pevzner, P. A. (2012). SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19(5), 455–477. https://doi.org/10.1089/cmb.2012.0021
Bano, I., Sajjad, H., Shah, A. M., Leghari, A., Mirbahar, K. H., Shams, S., & Soomro, M. (2016). A Review of Rabies Disease, its Transmission and Treatment. Journal of Animal Health and Production, 4(4), 140–144. https://doi.org/10.14737/journal.jahp/2016/4.4.140.144
Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Brito-Hoyos, D. M., Brito, E., & Villalobos, R. (2013). Distribución geográfica del riesgo de rabia de origen silvestre y evaluación de los factores asociados con su incidencia en Colombia, 1982-2010. Revista Panamericana de Salud Pública, 33(1), 8–14. https://doi.org/10.1590/s1020-49892013000100002
Brown, J., Pirrung, M., & McCue, L. A. (2017). FQC Dashboard: Integrates FastQC results into a web-based, interactive, and extensible FASTQ quality control tool. Bioinformatics, 33(19), 3137–3139. https://doi.org/10.1093/bioinformatics/btx373
Brunker, K., Nadin-Davis, S., & Biek, R. (2018). Genomic sequencing, evolution and molecular epidemiology of rabies virus. Revue Scientifique et Technique (International Office of Epizootics), 37(2), 401–408. https://doi.org/10.20506/rst.37.2.2810
Buchfink, B., Xie, C., & Huson, D. H. (2014). Fast and sensitive protein alignment using DIAMOND. Nature Methods, 12(1), 59–60. https://doi.org/10.1038/nmeth.3176
Calderón, A., Guzmán, C., Mattar, S., Rodríguez, V., Acosta, A., & Martínez, C. (2019). Frugivorous bats in the Colombian Caribbean region are reservoirs of the rabies virus. Annals of Clinical Microbiology and Antimicrobials, 18(1), 1–8. https://doi.org/10.1186/s12941-019-0308-y
Capobianchi, M. R., Giombini, E., & Rozera, G. (2013). Next-generation sequencing technology in clinical virology. Clinical Microbiology and Infection, 19(1), 15–22. https://doi.org/10.1111/1469-0691.12056
Cargnelutti, J. F., de Quadros, J. M., Martins, M., Batista, H. B. C. R., Weiblen, R., & Flores, E. F. (2017). Glycoprotein-G-gene-based molecular and phylogenetic analysis of rabies viruses associated with a large outbreak of bovine rabies in southern Brazil. Archives of Virology, 162(12), 3697–3704. https://doi.org/10.1007/s00705-017-3533-8
Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J., & Sayers, E. W. (2016). GenBank. Nucleic Acids Research, 44(D1), D67–D72. https://doi.org/10.1093/nar/gkv1276
de Almeida Campos, A. C., Romano, C. M., Melo, F. L., Araújo, D. B., Cunha, E. M. S., Sacramento, D. R. V., Durigon, E. L., & Lazarini, S. R. F. (2020). Phylogenetic analysis of near full-length sequences of the Desmodus rotundus genetic lineage of rabies virus. Infection, Genetics and Evolution, 80, 104179. https://doi.org/10.1016/j.meegid.2020.104179
Deforche, K. (2017). An alignment method for nucleic acid sequences against annotated genomes. BioRxiv, 200394. https://doi.org/10.1101/200394
Delmas, O., Holmes, E. C., Talbi, C., Larrous, F., Dacheux, L., Bouchier, C., & Bourhy, H. (2008). Genomic diversity and evolution of the lyssaviruses. PLoS ONE, 3(4), e2057. https://doi.org/10.1371/journal.pone.0002057
Desai, A., Marwah, V. S., Yadav, A., Jha, V., Dhaygude, K., Bangar, U., Kulkarni, V., & Jere, A. (2013). Identification of Optimum Sequencing Depth Especially for De Novo Genome Assembly of Small Genomes Using Next Generation Sequencing Data. PLoS ONE, 8(4), e60204. https://doi.org/10.1371/journal.pone.0060204
Desjardins, P., & Conklin, D. (2010). NanoDrop microvolume quantitation of nucleic acids. Journal of Visualized Experiments, 45, 1–4. https://doi.org/10.3791/2565
Drummond, A. J., Nicholls, G. K., Rodrigo, A. G., & Solomon, W. (2002). Estimating Mutation Parameters, Population History and Genealogy Simultaneously from Temporally Spaced Sequence Data. Genetics, 161, 1307–1320. https://doi.org/10.1093/genetics/161.3.1307
Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969–1973. https://doi.org/10.1093/molbev/mss075
Ellison, J. A., Gilbert, A. T., Recuenco, S., Moran, D., Alvarez, D. A., Kuzmina, N., Garcia, D. L., Peruski, L. F., Mendonça, M. T., Lindblade, K. A., & Rupprecht, C. E. (2014). Bat Rabies in Guatemala. PLoS Neglected Tropical Diseases, 8(7), e3070. https://doi.org/10.1371/journal.pntd.0003070
Escobar, L. E., Peterson, T., Favi, M., Yung, V., & Medina-Vogel, G. (2015). Bat-borne rabies in Latin America. Revista Do Instituto de Medicina Tropical de Sao Paulo, 57(1), 63–72. https://doi.org/10.1590/S0036-46652015000100009
Garcés-Ayala, F., Aréchiga-Ceballos, N., Ortiz-Alcántara, J. M., González-Durán, E., Pérez-Agüeros, S. I., Méndez-Tenorio, A., Torres-Longoria, B., López-Martínez, I., Hernández-Rivas, L., Díaz-Quiñonez, J. A., & Ramírez-González, J. E. (2017). Molecular characterization of atypical antigenic variants of canine rabies virus reveals its reintroduction by wildlife vectors in southeastern Mexico. Archives of Virology, 162(12), 3629–3637. https://doi.org/10.1007/s00705-017-3529-4
Gorbalenya, A. E., & Lauber, C. (2017). Phylogeny of Viruses. Reference Module in Biomedical Sciences. https://doi.org/10.1016/b978-0-12-801238-3.95723-4
Hall, T., Biosciences, I., & Carlsbad, C. (2011). BioEdit: An important software for molecular biology. GERF Bulletin of Biosciences, 2(1), 60–61.
Houldcroft, C. J., Beale, M. A., & Breuer, J. (2017). Clinical and biological insights from viral genome sequencing. Nature Reviews Microbiology, 15(3), 183–192. https://doi.org/10.1038/nrmicro.2016.182
Hutter, S. E., Brugger, K., Sancho V. H., González, R., Aguilar, O., León, B., Tichy, A., Firth, C. L., & Rubel, F. (2016). Rabies in Costa Rica: Documentation of the Surveillance Program and the Endemic Situation from 1985 to 2014. Vector-Borne and Zoonotic Diseases, 16(5), 334–341. https://doi.org/10.1089/vbz.2015.1906
Johnson, N., Aréchiga-Ceballos, N., & Aguilar-Setien, A. (2014). Vampire bat rabies: Ecology, epidemiology and control. Viruses, 6(5), 1911–1928. https://doi.org/10.3390/v6051911
Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780. https://doi.org/10.1093/molbev/mst010
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549. https://doi.org/10.1093/molbev/msy096
Kuzmin, I. V., Shi, M., Orciari, L. A., Yager, P. A., Velasco-Villa, A., Kuzmina, N. A., Streicker, D. G., Bergman, D. L., & Rupprecht, C. E. (2012). Molecular inferences suggest multiple host shifts of rabies viruses from bats to mesocarnivores in Arizona during 2001-2009. PLoS Pathogens, 8(6), e1002786. https://doi.org/10.1371/journal.ppat.1002786
Lavergne, A., Darcissac, E., Bourhy, H., Tirera, S., de Thoisy, B., & Lacoste, V. (2016). Complete genome sequence of a vampire bat rabies virus from French Guiana. Genome Announcements, 4(2), e00188-16. https://doi.org/10.1128/genomeA.00188-16
León, B., Fallas González, S., Miranda Solís, L., Ramírez-Cardoce, M., Moreira-Soto, A., Cordero-Solórzano, J. M., Elisabeth Hutter, S., González-Barrientos, R., & Rupprecht, C. E. (2021). Rabies in Costa Rica – Next Steps Towards Controlling Bat-Borne Rabies After its Elimination in Dogs. Yale Journal of Biology and Medicine, 94(2), 311-329.
Marston, D. A., McElhinney, L. M., Ellis, R. J., Horton, D. L., Wise, E. L., Leech, S. L., David, D., de Lamballerie, X., & Fooks, A. R. (2013). Next generation sequencing of viral RNA genomes. BMC Genomics, 14(1), 1-12. https://doi.org/10.1186/1471-2164-14-444
Martin, D. P., Murrell, B., Golden, M., Khoosal, A., & Muhire, B. (2015). RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evolution, 1(1), vev003. https://doi.org/10.1093/ve/vev003
Maurier, F., Beury, D., Fléchon, L., Varré, J.-S., Touzet, H., Goffard, A., Hot, D., & Caboche, S. (2019). A complete protocol for whole-genome sequencing of virus from clinical samples: Application to coronavirus OC43. Virology, 531, 141–148. https://doi.org/10.1016/j.virol.2019.03.006
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). 2010 Gateway Computing Environments Workshop, GCE 2010. 2010 Gateway Computing Environments Workshop, GCE 2010.
Mochizuki, N., Kobayashi, Y., Sato, G., Hirano, S., Itou, T., Ito, F. H., & Sakai, T. (2011). Determination and molecular analysis of the complete genome sequence of two wild-type rabies viruses isolated from a haematophagous bat and a frugivorous bat in Brazil. Journal of Veterinary Medical Science, 73(6), 759–766. https://doi.org/10.1292/jvms.10-0238
Moser, L. A., Ramirez-Carvajal, L., Puri, V., Pauszek, S. J., Matthews, K., Dilley, K. A., Mullan, C., McGraw, J., Khayat, M., Beeri, K., Yee, A., Dugan, V., Heise, M.T., Frieman, M.B., Rodriguez, L.L., Bernard, K.A., Wentworth, D.E., Stockwell, T.B., Shabman, R.S. (2016). A universal next-generation sequencing protocol to generate noninfectious containment RNA viruses. MSystems, 1(3), e00039-15. https://doi.org/10.1128/mSystems.00039-15
NCBI Resource Coordinators. (2018). Database resources of the National Center for Biotechnology Information. Nucleic Acids Research, 46(D1), D8-D13. https://doi.org/10.1093/nar/gkx1095
Oyola, S. O., Gu, Y., Manske, M., Otto, T. D., O’Brien, J., Alcock, D., MacInnis, B., Berriman, M., Newbold, C. I., Kwiatkowski, D. P., Swerdlow, H. P., & Quail, M. A. (2013). Efficient depletion of host DNA contamination in malaria clinical sequencing. Journal of Clinical Microbiology, 51(3), 745–751. https://doi.org/10.1128/JCM.02507-12
Sadeuh-Mba, S. A., Momo, J. B., Besong, L., Loul, S., & Njouom, R. (2017). Molecular characterization and phylogenetic relatedness of dog-derived Rabies Viruses circulating in Cameroon between 2010 and 2016. PLoS Neglected Tropical Diseases, 11(10), 1–21. https://doi.org/10.1371/journal.pntd.0006041
Salomão, C., Nacima, A., Cuamba, L., Gujral, L., Amiel, O., Baltazar, C., Cliff, J., & Gudo, E. S. (2017). Epidemiology, clinical features and risk factors for human rabies and animal bites during an outbreak of rabies in Maputo and Matola cities, Mozambique, 2014: Implications for public health interventions for rabies control. PLoS Neglected Tropical Diseases, 11(7), 1–16. https://doi.org/10.1371/journal.pntd.0005787
Soltis, P. S., & Soltis, D. E. (2003). Applying the Bootstrap in Phylogeny Reconstruction. Statistical Science, 18(2), 256–267. https://doi.org/10.1214/ss/1063994980
Streicker, D. G., Fallas González, S. L., Luconi, G., Barrientos, R. G., & Leon, B. (2019). Phylodynamics reveals extinction–recolonization dynamics underpin apparently endemic vampire bat rabies in Costa Rica. Proceedings of the Royal Society B: Biological Sciences, 286(1912). https://doi.org/10.1098/rspb.2019.1527
Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22(22), 4673–4680. https://doi.org/10.1093/nar/22.22.4673
Vilsker, M., Moosa, Y., Nooij, S., Fonseca, V., Ghysens, Y., Dumon, K., Pauwels, R., Alcantara, L. C., Vanden Eynden, E., Vandamme, A. M., Deforche, K., & de Oliveira, T. (2019). Genome Detective: An automated system for virus identification from high-throughput sequencing data. Bioinformatics, 35(5), 871–873. https://doi.org/10.1093/bioinformatics/bty695
Yaguana, J., & López, M. (2017). La Rabia canina: Su historia, epidemiología y sus medidas de control. Revista Electrónica de Veterinaria, 18(9), 1-13.
Published
How to Cite
Issue
Section
License
Copyright (c) 2021 UNED Research Journal
This work is licensed under a Creative Commons Attribution 4.0 International License.
Note: This abstract contains an incorrect copyright due to technical issues. Authors who publish with this journal agree to the following terms: Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal
All journal contents are freely available through a CC BY 4.0 license.
CC BY 4.0 is a Creative Commons: you can copy, modify, distribute, and perform, even for commercial reasons, without asking permission, if you give appropriate credit.
Contents can be reproduced if the source and copyright are acknowledged according to the Open Access license CC BY 4.0. Self-storage in preprint servers and repositories is allowed for all versions. We encourage authors to publish raw data and data logs in public repositories and to include the links with all drafts so that reviewers and readers can consult them at any time.
The journal is financed by public funds via Universidad Estatal a Distancia and editorial independence and ethical compliance are guaranteed by the Board of Editors, UNED. We do not publish paid ads or receive funds from companies.