Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders - PubMed (original) (raw)
Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders
H Badrane et al. J Virol. 2001 Sep.
Abstract
Lyssaviruses are unsegmented RNA viruses causing rabies. Their vectors belong to the Carnivora and Chiroptera orders. We studied 36 carnivoran and 17 chiropteran lyssaviruses representing the main genotypes and variants. We compared their genes encoding the surface glycoprotein, which is responsible for receptor recognition and membrane fusion. The glycoprotein is the main protecting antigen and bears virulence determinants. Point mutation is the main force in lyssavirus evolution, as Sawyer's test and phylogenetic analysis showed no evidence of recombination. Tests of neutrality indicated a neutral model of evolution, also supported by globally high ratios of synonymous substitutions (d(S)) to nonsynonymous substitutions (d(N)) (>7). Relative-rate tests suggested similar rates of evolution for all lyssavirus lineages. Therefore, the absence of recombination and similar evolutionary rates make phylogeny-based conclusions reliable. Phylogenetic reconstruction strongly supported the hypothesis that host switching occurred in the history of lyssaviruses. Indeed, lyssaviruses evolved in chiropters long before the emergence of carnivoran rabies, very likely following spillovers from bats. Using dated isolates, the average rate of evolution was estimated to be roughly 4.3 x 10(-4) d(S)/site/year. Consequently, the emergence of carnivoran rabies from chiropteran lyssaviruses was determined to have occurred 888 to 1,459 years ago. Glycoprotein segments accumulating more d(N) than d(S) were distinctly detected in carnivoran and chiropteran lyssaviruses. They may have contributed to the adaptation of the virus to the two distinct mammal orders. In carnivoran lyssaviruses they overlapped the main antigenic sites, II and III, whereas in chiropteran lyssaviruses they were located in regions of unknown functions.
Figures
FIG. 1
Lyssavirus-rooted phylogenetic tree. The tree was estimated using the neighbor-joining method (39) on the basis of the ECTO nucleotide sequence. Bootstrap values of 1,000 replicates indicate the robustness of the corresponding node. The sequences retrieved from GenBank and those described in the work of Badrane et al. (3) are marked with * and †, respectively. RABV, Rabies virus; EBLV-1, European bat lyssavirus 1; EBLV-2, European bat lyssavirus 2; ABLV, Australian bat lyssavirus; DUVV, Duvenhage virus; LBV, Lagos bat virus; MOKV, Mokola virus.
FIG. 2
Ratios of dN to dS along the G gene coding region. We plotted the d S/d N ratio for each pairwise comparison (17) of chiropteran (top graph) and carnivoran (bottom graph) lyssaviruses along their G gene coding regions. Threshold lines of the significance of the ratios are shown at values 1 and 2. A schematic representation of the G gene shows the different domains, SP, TM, ENDO, and ECTO, where antigenic sites are indicated with vertical black boxes. Horizontal black or open boxes represent regions of the chiropteran or carnivoran lyssavirus G gene, respectively, which accumulate significantly more d N than d S. *, d N > d S and d N ≤ 1; **, d N > 2_d_ S and d N ≤ 1.
FIG. 3
Lyssavirus phylogenetic tree with a molecular clock (PHYLIP phylogeny inference package) derived from nonsynonymous corrected distances (23). Six of the seven Lyssavirus GTs are represented (except GT3). Bold branches distinguish chiropteran Lyssavirus lineages. The geographic locations and vectors of RABV main lineages are indicated. Curved arrows symbolize the two spillover events. Timing estimations of spillovers and of the most recent Lyssavirus ancestor are indicated on the scale.
Similar articles
- Bat lyssaviruses.
Markotter W, Coertse J. Markotter W, et al. Rev Sci Tech. 2018 Aug;37(2):385-400. doi: 10.20506/rst.37.2.2809. Rev Sci Tech. 2018. PMID: 30747140 English. - Antigenic site changes in the rabies virus glycoprotein dictates functionality and neutralizing capability against divergent lyssaviruses.
Evans JS, Selden D, Wu G, Wright E, Horton DL, Fooks AR, Banyard AC. Evans JS, et al. J Gen Virol. 2018 Feb;99(2):169-180. doi: 10.1099/jgv.0.000998. Epub 2018 Jan 4. J Gen Virol. 2018. PMID: 29300155 - Utilisation of Chimeric Lyssaviruses to Assess Vaccine Protection against Highly Divergent Lyssaviruses.
Evans JS, Wu G, Selden D, Buczkowski H, Thorne L, Fooks AR, Banyard AC. Evans JS, et al. Viruses. 2018 Mar 15;10(3):130. doi: 10.3390/v10030130. Viruses. 2018. PMID: 29543715 Free PMC article. - Rabies: epidemiological tendencies and control tools.
Tordo N, Bahloul C, Jacob Y, Jallet C, Perrin P, Badrane H. Tordo N, et al. Dev Biol (Basel). 2006;125:3-13. Dev Biol (Basel). 2006. PMID: 16878455 Review. - A perspective on lyssavirus emergence and perpetuation.
Rupprecht CE, Turmelle A, Kuzmin IV. Rupprecht CE, et al. Curr Opin Virol. 2011 Dec;1(6):662-70. doi: 10.1016/j.coviro.2011.10.014. Epub 2011 Nov 10. Curr Opin Virol. 2011. PMID: 22440925 Review.
Cited by
- Sex Bias in Sample Collections From Bats, the Culprit of SARS Coronavirus, SARS-Coronavirus-2, and Other Emerging Viruses.
Lau SKP, He Z, Lin KPK, Woo PCY. Lau SKP, et al. Infect Microbes Dis. 2020 Oct 6;2(4):173-174. doi: 10.1097/IM9.0000000000000036. eCollection 2020 Dec. Infect Microbes Dis. 2020. PMID: 38630082 Free PMC article. No abstract available. - Fifty Years of the National Rabies Control Program in Brazil under the One Health Perspective.
Schneider MC, Min KD, Romijn PC, De Morais NB, Montebello L, Manrique Rocha S, Sciancalepore S, Hamrick PN, Uieda W, Câmara VM, Luiz RR, Belotto A. Schneider MC, et al. Pathogens. 2023 Nov 11;12(11):1342. doi: 10.3390/pathogens12111342. Pathogens. 2023. PMID: 38003806 Free PMC article. - Phylogeographic Aspects of Bat Lyssaviruses in Europe: A Review.
Dundarova H, Ivanova-Aleksandrova N, Bednarikova S, Georgieva I, Kirov K, Miteva K, Neov B, Ostoich P, Pikula J, Zukal J, Hristov P. Dundarova H, et al. Pathogens. 2023 Aug 27;12(9):1089. doi: 10.3390/pathogens12091089. Pathogens. 2023. PMID: 37764897 Free PMC article. Review. - Evolution and distribution of rabies viruses from a panorama view.
Li G, Zhang Y, He HL, Chen CY, Li X, Xiao Y, Yan ZB, Chu Y, Luo J, Guo XF. Li G, et al. Microbiol Spectr. 2023 Sep 5;11(5):e0525722. doi: 10.1128/spectrum.05257-22. Online ahead of print. Microbiol Spectr. 2023. PMID: 37668395 Free PMC article.
References
- Aaziz R, Tepfer M. Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol. 1999;80:1339–1346. - PubMed
- Aitken T H, Kowalski R W, Beaty B J, Buckley S M, Wright J D, Shope R E, Miller B R. Arthropod studies with rabies-related Mokola virus. Am J Trop Med Hyg. 1984;33:945–952. - PubMed
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources