Genomic Diversity and Evolution of the Lyssaviruses

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2008 May 1

PMID 18446239

Citations 79

Authors

Olivier Delmas

Edward C Holmes

Chiraz Talbi

Florence Larrous

Laurent Dacheux

Christiane Bouchier

Herve Bourhy

Affiliations

Soon will be listed here.

Abstract

Lyssaviruses are RNA viruses with single-strand, negative-sense genomes responsible for rabies-like diseases in mammals. To date, genomic and evolutionary studies have most often utilized partial genome sequences, particularly of the nucleoprotein and glycoprotein genes, with little consideration of genome-scale evolution. Herein, we report the first genomic and evolutionary analysis using complete genome sequences of all recognised lyssavirus genotypes, including 14 new complete genomes of field isolates from 6 genotypes and one genotype that is completely sequenced for the first time. In doing so we significantly increase the extent of genome sequence data available for these important viruses. Our analysis of these genome sequence data reveals that all lyssaviruses have the same genomic organization. A phylogenetic analysis reveals strong geographical structuring, with the greatest genetic diversity in Africa, and an independent origin for the two known genotypes that infect European bats. We also suggest that multiple genotypes may exist within the diversity of viruses currently classified as 'Lagos Bat'. In sum, we show that rigorous phylogenetic techniques based on full length genome sequence provide the best discriminatory power for genotype classification within the lyssaviruses.

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References

Faber M, Pulmanausahakul R, Nagao K, Prosniak M, Rice A, Koprowski H . Identification of viral genomic elements responsible for rabies virus neuroinvasiveness. Proc Natl Acad Sci U S A. 2004; 101(46):16328-32. PMC: 528969. DOI: 10.1073/pnas.0407289101. View

Davis P, Bourhy H, Holmes E . The evolutionary history and dynamics of bat rabies virus. Infect Genet Evol. 2006; 6(6):464-73. DOI: 10.1016/j.meegid.2006.02.007. View

Emonet S, Grard G, Brisbarre N, Moureau G, Temmam S, Charrel R . Long PCR Product Sequencing (LoPPS): a shotgun-based approach to sequence long PCR products. Nat Protoc. 2007; 2(2):340-6. DOI: 10.1038/nprot.2006.453. View

Tordo N, Poch O, Ermine A, Keith G, Rougeon F . Completion of the rabies virus genome sequence determination: highly conserved domains among the L (polymerase) proteins of unsegmented negative-strand RNA viruses. Virology. 1988; 165(2):565-76. DOI: 10.1016/0042-6822(88)90600-9. View

Bourhy H, Kissi B, Audry L, Smreczak M, Sadkowska-Todys M, Kulonen K . Ecology and evolution of rabies virus in Europe. J Gen Virol. 1999; 80 ( Pt 10):2545-2557. DOI: 10.1099/0022-1317-80-10-2545. View

Arai Y, Kuzmin I, Kameoka Y, Botvinkin A . New lyssavirus genotype from the Lesser Mouse-eared Bat (Myotis blythi), Kyrghyzstan. Emerg Infect Dis. 2003; 9(3):333-7. PMC: 2958534. DOI: 10.3201/eid0903.020252. View

Le Mercier P, Jacob Y, Tordo N . The complete Mokola virus genome sequence: structure of the RNA-dependent RNA polymerase. J Gen Virol. 1997; 78 ( Pt 7):1571-6. DOI: 10.1099/0022-1317-78-7-1571. View

Marston D, McElhinney L, Johnson N, Muller T, Conzelmann K, Tordo N . Comparative analysis of the full genome sequence of European bat lyssavirus type 1 and type 2 with other lyssaviruses and evidence for a conserved transcription termination and polyadenylation motif in the G-L 3' non-translated region. J Gen Virol. 2007; 88(Pt 4):1302-1314. DOI: 10.1099/vir.0.82692-0. View

Kissi B, Tordo N, Bourhy H . Genetic polymorphism in the rabies virus nucleoprotein gene. Virology. 1995; 209(2):526-37. DOI: 10.1006/viro.1995.1285. View

10.

Bourhy H, Kissi B, Tordo N . Molecular diversity of the Lyssavirus genus. Virology. 1993; 194(1):70-81. DOI: 10.1006/viro.1993.1236. View

11.

Kosakovsky Pond S, Frost S . Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics. 2005; 21(10):2531-3. DOI: 10.1093/bioinformatics/bti320. View

12.

Wu X, Franka R, Velasco-Villa A, Rupprecht C . Are all lyssavirus genes equal for phylogenetic analyses?. Virus Res. 2007; 129(2):91-103. DOI: 10.1016/j.virusres.2007.06.022. View

13.

Botvinkin A, Poleschuk E, Kuzmin I, Borisova T, Gazaryan S, Yager P . Novel lyssaviruses isolated from bats in Russia. Emerg Infect Dis. 2004; 9(12):1623-5. PMC: 3034350. DOI: 10.3201/eid0912.030374. View

14.

Auewarakul P . Composition bias and genome polarity of RNA viruses. Virus Res. 2005; 109(1):33-7. PMC: 7114242. DOI: 10.1016/j.virusres.2004.10.004. View

15.

Gifford R, de Oliveira T, Rambaut A, Myers R, Gale C, Dunn D . Assessment of automated genotyping protocols as tools for surveillance of HIV-1 genetic diversity. AIDS. 2006; 20(11):1521-9. DOI: 10.1097/01.aids.0000237368.64488.ae. View

16.

Gould A, Kattenbelt J, Gumley S, Lunt R . Characterisation of an Australian bat lyssavirus variant isolated from an insectivorous bat. Virus Res. 2002; 89(1):1-28. DOI: 10.1016/s0168-1702(02)00056-4. View

17.

Bourhy H, Cowley J, Larrous F, Holmes E, Walker P . Phylogenetic relationships among rhabdoviruses inferred using the L polymerase gene. J Gen Virol. 2005; 86(Pt 10):2849-2858. DOI: 10.1099/vir.0.81128-0. View

18.

Holmes E, Woelk C, Kassis R, Bourhy H . Genetic constraints and the adaptive evolution of rabies virus in nature. Virology. 2002; 292(2):247-57. DOI: 10.1006/viro.2001.1271. View

19.

Tordo N, Poch O, Ermine A, Keith G, Rougeon F . Walking along the rabies genome: is the large G-L intergenic region a remnant gene?. Proc Natl Acad Sci U S A. 1986; 83(11):3914-8. PMC: 323635. DOI: 10.1073/pnas.83.11.3914. View

20.

Davis P, Holmes E, Larrous F, van der Poel W, Tjornehoj K, Alonso W . Phylogeography, population dynamics, and molecular evolution of European bat lyssaviruses. J Virol. 2005; 79(16):10487-97. PMC: 1182613. DOI: 10.1128/JVI.79.16.10487-10497.2005. View