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Dispersion and diversification of Lyssavirus rabies transmitted from haematophagous bats Desmodus rotundus: a phylogeographical study

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Abstract

Rabies is worldwide zoonosis caused by Lyssavirus rabies (RABV) a RNA negative sense virus with low level of fidelity during replication cycle. Nucleoprotein of RABV is the most conserved between all five proteins of the virus and is the most used gene for phylogenetic and phylogeographic studies. Despite of rabies been very important in Public Health concern, it demands continuous prophylactic care for herbivores with economic interest, such as cattle and horses. The main transmitter of RABV for these animals in Brazil is the hematophagous bats Desmodus rotundus. The aim of this study was to determine the dispersion over time and space of RABV transmitted by D. rotundus. Samples of RABV from the State of São Paulo (SP), Southeast Brazil isolated from the central nervous system (CNS) of cattle, were submitted to RNA extraction, RT-PCR, sequencing and phylogeographic analyzes with BEAST (Bayesian Evolutionary Analysis Sampling Trees) v 2.5 software. Was possible to identify high rate of diversification in starts sublineages of RABV what are correlated with a behavior of D. rotundus, the main transmitter of rabies to cattle. This study also highlights the importance of continuous monitoring of genetic lineages of RABV in Brazil.

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References

  1. Carnieli P Jr, Castilho JG, de Fahl WO, Véras NMC, do Timenetsky MCST (2009) Genetic characterization of Rabies virus isolated from cattle between 1997 and 2002 in an epizootic area in the state of São Paulo, Brazil. Virus Res 144:215–224

    Article  CAS  PubMed  Google Scholar 

  2. Castilho JG, Carnieli P Jr, Durymanova EA, de Fahl WO, de Oliveira RN, Macedo CI, da Rosa EST, Mantilla A, Carrieri ML, Kotait I (2010) Human rabies transmitted by vampire bats: antigenic and genetic characterization of rabies virus isolates from the Amazon region (Brazil and Ecuador). Virus Res 153:100–105

    Article  CAS  PubMed  Google Scholar 

  3. Benavides JA, Valderrama W, Recuenco S, Uieda W, Suzán G, Avila-Flores R, Velasco-Villa A, Almeida M, de Andrade FAG, Molina-Flores B, Vigilato MAN, Pompei JCA, Tizzani P, Carrera JE, Ibanez D, Streicker DG (2020) Defining new pathways to manage the ongoing emergence of bat rabies in Latin America. Viruses 12:1002

    Article  PubMed  PubMed Central  Google Scholar 

  4. Whelan SPJ, Wertz GW (1999) Regulation of RNA synthesis by the genomic termini of vesicular stomatitis virus: identification of distinct sequences essential for transcription but not replication. J Virol 73:297–306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Holmes EC, Woelk CH, Kassis R, Bourhyt H (2002) Genetic constraints and the adaptive evolution of rabies virus in nature. Virology 292:247–257

    Article  CAS  PubMed  Google Scholar 

  6. Real LA, Henderson JC, Biek R, Snaman J, Jack TL, Childs JE, Stahl E, Waller L, Tinline R, Nadin-Davis S (2005) Unifying the spatial population dynamics and molecular evolution of epidemic rabies virus. Proc Natl Acad Sci USA 102:12107–12111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. An M, Han X, Zhao B, English S, Frost SDW, Zhang H, Shang H (2020) Cross-continental dispersal of major HIV-1 CRF01_AE clusters in China. Front Microbiol 11:61

    Article  PubMed  PubMed Central  Google Scholar 

  8. Srihi H, Chatti N, Mhadheb MB, Gharbi J, Abid N (2021) Phylodynamic and phylogeographic analysis of the complete genome of the West Nile virus lineage 2 (WNV-2) in the Mediterranean basin. BMC Ecol Evo 21:183

    Article  Google Scholar 

  9. Streicker D, Winternitz JC, Satterfield C-C, Broos A, Tello C, Recuenco S, Velasco-Villa A, Altizer S, Valderrama W (2016) Host–pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies. Proc Natl Acad Sci USA 113:10926–10931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Kuzmina NA, Lemey P, Kuzmin IV, Mayes BC, Ellison JA, Orciari LA, Hightower D, Taylor ST, Rupprecht CE (2013) The phylogeography and spatiotemporal spread of south-central skunk rabies virus. PloS one 8:e82348

    Article  PubMed  PubMed Central  Google Scholar 

  11. Brunker K, Marston DA, Horton DL, Cleaveland S, Fooks AR, Kazwala R, Ngeleja C, Lembo T, Sambo M, Mtema ZJ, Sikana L, Wilkie G, Biek R, Hampson K (2015) Elucidating the phylodynamics of endemic rabies virus in eastern Africa using whole-genome sequencing. Virus Evol 1:vev011

    Article  PubMed  PubMed Central  Google Scholar 

  12. Nahata KD, Bollen N, Gill MS, Layan M, Bourhy H, Dellicour S, Baele G (2021) On the use of phylogeographic inference to infer the dispersal history of rabies virus: a review study. Viruses 13:1628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Carnieli P Jr, de Oliveira RN, Macedo CI, Castilho JG (2011) Phylogeography of rabies virus isolated from dogs in Brazil between 1985 and 2006. Arch Virol 156:1007–1012

    Article  CAS  PubMed  Google Scholar 

  14. Carnieli P Jr, Batista HBCR, de Oliveira RN, Castilho JG, Vieira LFP (2013) Phylogeographic dispersion and diversification of rabies virus lineages associated with dogs and crab-eating foxes (Cerdocyon thous) in Brazil. Arch Virol 158:2307–2313

    Article  CAS  PubMed  Google Scholar 

  15. Vieira LFP, Pereira SRFG, Carnieli P Jr, Tavares LCB, Kotait I (2013) Phylogeography of rabies virus isolated from herbivores and bats in the Espírito Santo State, Brazil. Virus Genes 46:330–336

    Article  CAS  PubMed  Google Scholar 

  16. Orciari L, Niezgoda M, Hanlon CA, Shaddock JH, Sanderlin DW, Yager PA, Rupprecht CE (2001) Rapid clearance of SAG-2 rabies virus from dogs after oral vaccination. Vaccine 19:4511–4518

    Article  CAS  PubMed  Google Scholar 

  17. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  18. Bouckaert R, Vaughan T, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, Matschiner M, Mendes FK, Müller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Suchard MA, Wu CH, Xie D, Zhang C, Stadler T, Drummond AJ (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PloS Comput Biol 15:e1006650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bouckaert RR, Drummond AJ (2017) bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evol Biol 17:42

    Article  PubMed  PubMed Central  Google Scholar 

  20. Bouckaert R (2016) Phylogeography by diffusion on a sphere: whole world phylogeography. PeerJ 4:e2406

    Article  PubMed  PubMed Central  Google Scholar 

  21. Raumbaut A (2018) FigTree: Tree Figure Drawing Tool version 1.4.4. Institute of Evolutionary Biology, University of Edinburgh. https://github.com/rambaut/figtree/releases. Accessed 27 Jan 2023

  22. Bielejec F, Rambaut A, Suchard MA, Lemey P (2011) SPREAD: spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics 27:2910–2912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using tracer. Syst Biol 17(67):901–904

    Article  Google Scholar 

  24. De Benedictis P, Leopardi S, Markotter W, Velasco-Villa A (2022) The importance of accurate host species identification in the framework of rabies surveillance, control and elimination. Viruses 14:492

    Article  PubMed  PubMed Central  Google Scholar 

  25. Grigorescu F, Lautier C (2020) How geneticists contribute to understanding of covid-19 disease pathogenicity. Acta Endocrinol (Buchar) 16:346–352

    Article  CAS  PubMed  Google Scholar 

  26. Nguyen PT, Kant R, Broeck FVD, Suvanto MT, Alburkat H, Virtanen J, Ahvenainen E, Castren R, Hong SL, Baele G, Ahava MJ, Jarva H, Jokiranta ST, Kallio-kokko H, Kekäläinen E, Kirjavainen V, Kortela E, Kurkela S, Lappalainen M, Liimatainen H, Suchard MA, Hannula S, Ellonen P, Sironen T, Lemey P, Vapalahti O, Smura T (2022) The phylodynamics of SARS-CoV-2 during 2020 in Finland. Commun Med (Lond) 2:65

    Article  Google Scholar 

  27. Duchatel F, Bronsvoort BMC, Lycett S (2019) Phylogeographic analysis and identification of factors impacting the diffusion of foot-and-mouth disease virus in africa. Front Ecol Evol 7:371

    Article  Google Scholar 

  28. de Oliveira RN, de Souza SP, Lobo RSV, Castilho JG, Macedo CI, Carnieli P Jr, Fahl WO, Achkar SM, Scheffer KC, Kotait I, Carrieri ML, Brandão PE (2010) Rabies virus in insectivorous bats: Implications of the diversity of the nucleoprotein and glycoprotein genes for molecular epidemiology. Virology 405:352–360

    Article  CAS  PubMed  Google Scholar 

  29. Schaefer R, Batista HBR, Franco AC, Rijsewijk FAM, Roehe PM (2005) Studies on antigenic and genomic properties of Brazilian rabies virus isolates. Vet Microbiol 107:161–170

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was supported by a grant from FAPESP, Brazil, in 2017 (Project Code No. 2017/06089-4) and the Pasteur Institute of São Paulo—Secretary of State for Health of São Paulo.

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Authors and Affiliations

  1. Pasteur Institute of São Paulo, São Paulo, Brazil

    Helena Beatriz de Carvalho Ruthner Batista, Juliana Galera Castilho Kawai, Willian de Oliveira Fahl, Camila Mosca Barboza, Samira Achkar, Rafael de Novaes Oliveira & Pedro Carnieli Junior

  2. School of Veterinary Medicine, University of São Paulo, São Paulo, Brazil

    Paulo Eduardo Brandão

  3. Institute of Agricultural and Forestry Defense of the State of Espirito Santo, São Paulo, Brazil

    Luiz Fernando Pereira Vieira

Authors
  1. Helena Beatriz de Carvalho Ruthner Batista
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  2. Luiz Fernando Pereira Vieira
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  3. Juliana Galera Castilho Kawai
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  4. Willian de Oliveira Fahl
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  5. Camila Mosca Barboza
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  7. Rafael de Novaes Oliveira
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  8. Paulo Eduardo Brandão
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  9. Pedro Carnieli Junior
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Contributions

PCJr. conceived and designed the experiments; JGCK, WOF, SMA, CMB and RNO performed practical experiments; HBCRB, LFV, PEB and PCJr., performed the analysis of sequences; HBCRB and PCJr wrote the manuscript and prepared the figures. All authors reviewed and approved the final manuscript.

Corresponding author

Correspondence to Helena Beatriz de Carvalho Ruthner Batista.

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Edited by Zhen Fu.

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de Carvalho Ruthner Batista, H.B., Vieira, L.F.P., Kawai, J.G.C. et al. Dispersion and diversification of Lyssavirus rabies transmitted from haematophagous bats Desmodus rotundus: a phylogeographical study. Virus Genes 59, 817–822 (2023). https://doi.org/10.1007/s11262-023-02030-x

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