1 Rabies Laboratory, WHO Collaborating Centre for Reference and Research on Rabies, Institut Pasteur, 28 rue du docteur Roux, 75724 Paris Cedex 15, France
2 CSIRO Livestock Industries, Queensland Bioscience Precinct, 306 Carmody Road, St Lucia, QLD 4067, Australia
3 Department of Biology, The Pennsylvania State University, Mueller Laboratory, University Park, PA 16802, USA
4 CSIRO Livestock Industries, Australian Animal Health Laboratory, 5 Portarlington Road, Geelong, VIC 3220, Australia
Correspondence
H. Bourhy
hbourhy{at}pasteur.fr
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ABSTRACT |
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INTRODUCTION |
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All rhabdoviruses contain a single-stranded () RNA genome which encodes five virion structural proteins: the nucleoprotein (N), the phosphoprotein (P), the matrix protein (M), the glycoprotein (G) and the polymerase (L) (Dale & Peters, 1981). An added layer of complexity is present in the genus Ephemerovirus, as these viruses contain several additional open reading frames (ORFs) between the G and L genes which encode a second glycoprotein (GNS) and several other non-structural proteins (Walker et al., 1992
, 1994
; Wang et al., 1994
; McWilliam et al., 1997
). Similarly, in the genus Novirhabdovirus, a sixth functional cistron between the G and L genes encodes a non-structural protein (NV) of unknown function (Basurco & Benmansour, 1995
). The unclassified rhabdovirus Sigma virus of Drosophila and plant rhabdoviruses in the genera Cytorhabdovirus and Nucleorhabdovirus also contain an additional ORF, which is located between the P and M genes (Heaton et al., 1989
; Landes-Devauchelle et al., 1995
; Wetzel et al., 1994
).
The available gene-sequence data from rhabdoviruses has increased considerably in recent years and this, in conjunction with data on genome organization and a variety of other biological characteristics, has been used for taxonomic classification and species demarcation among the Vesiculovirus, Lyssavirus, Ephemerovirus and Novirhabdovirus genera. In particular, the subdivision of each genus into species is supported by the comparison of nucleotide and deduced amino acid sequences of one (N gene) or several (N and G) common genes (Badrane & Tordo, 2001; Barr et al., 1991
; Basurco et al., 1995
; Bourhy et al., 1993
; Crysler et al., 1990
; Kissi et al., 1995
; Masters & Banerjee, 1987
; Walker et al., 1994
; Wang et al., 1995
). However, complete genome sequences are available for only a few type species and it is unlikely that such data will be sought for the vast number of unclassified rhabdoviruses: a list of 63 unassigned animal rhabdoviruses is presented in the eighth International Committee on Taxonomy of Viruses (ICTV) report, a further 29 have been only tentatively assigned to genera due to inadequate data (Tordo et al., 2004
), and many more are awaiting classification.
One approach to the determination of the phylogenetic relationships among the Rhabdoviridae, as well as the identification of new viral species, is to utilize the conserved amino acid sequence blocks and/or motifs that have been identified in alignments of the RNA-dependent RNA polymerase (L protein) (Bock et al., 2004; Delarue et al., 1990
; Dhillon et al., 2000
; Elliott et al., 1992
; Müller et al., 1994
; Le Mercier et al., 1997
; Poch et al., 1989
, 1990
; Tordo et al., 1988
; Vieth et al., 2004
). Block III of the L polymerase is predicted to be essential for RNA polymerase function because it is conserved among all RNA-dependent RNA polymerases (Delarue et al., 1990
; Poch et al., 1989
; Xiong & Eickbush, 1990
) and mutations in this region abolish polymerase activity (Schnell & Conzelmann, 1995
; Sleat & Banerjee, 1993
; Jin & Elliott, 1991
, 1992
). The sequence conservation displayed by this region suggests that it may be a useful target for the exploration of distant evolutionary relationships among the vast array of unclassified rhabdoviruses.
In this study, we inferred the phylogenetic relationships among 56 rhabdoviruses, 20 of which are currently tentative species or unassigned within the Rhabdoviridae. This represents the largest phylogenetic study of the Rhabdoviridae undertaken to date. Degenerate primers targeting block III of the L gene were defined and used for RT-PCR and sequence analysis, providing a rapid and expansive method to investigate the phylogenetic relationships. The broader goal of this research is to merge phylogenetic and epidemiological information, such as the host and vector species, to provide a more accurate and complete picture of the evolution of key biological characteristics within the Rhabdoviridae.
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METHODS |
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Phylogenetic analysis.
The dataset of 38 rhabdovirus sequences newly determined here was compared with the corresponding block III L polymerase amino acid sequences of 18 rhabdoviruses collected from GenBank (Table 1). All amino acid sequences were aligned using the CLUSTAL W programme (Thompson et al., 1994
) and then checked for accuracy by eye. This resulted in a final alignment of sequences of 158 amino acid residues in length (Fig. 1
).
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RESULTS AND DISCUSSION |
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Primers PVO3 and PVO4 produced PCR products for 38 animal rhabdoviruses, 20 of which are not currently assigned to a particular genus (Table 1). These primers amplified a 456462 nucleotide region, conforming to the expected size. Internal primers PVO5 (5'-ATGACGGACAAYCTGAACAA-3', position 71707189) and PVO6 (5'-CCRTTCCARCAGGTAGGDCC-3', position 74867467) were used for sequencing some PCR products. These primers amplified a 317 nucleotide region.
Sequence analysis of L polymerase block III
A total of 56 rhabdovirus L polymerase sequences were subjected to phylogenetic analysis (Table 1). These sequences encompass the three highly conserved segments (pre-motif A, motif A and motif B) of block III of the L polymerase (Fig. 2
), which is present in all the RNA-dependent RNA polymerases studied so far, including reverse transcriptase (Poch et al., 1989
; Xiong & Eickbush, 1990
). Although these sequences are extremely divergent, sufficient sequence similarity exists in some domains of the rhabdovirus polymerases to make phylogenetic analysis possible (Dhillon et al., 2000
; Le Mercier et al., 1997
; Müller et al., 1994
; Vieth et al., 2004
). Importantly, the alignment confirmed the conservation of some residues among all the Rhabdoviridae (Le Mercier et al., 1997
; Müller et al., 1994
), whilst also identifying new residues that are conserved among the Mononegavirales (Fig. 2
).
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Phylogenetic analysis of the Rhabdoviridae using the sequence of block III
Previously, taxonomic relationships among members of the Rhabdoviridae were primarily based on structural properties (genome size and complexity), large-scale biological properties (host range, epidemiological cycles, routes of transmission) and serological cross-reactions (immunofluorescence, complement fixation (CF), neutralization tests). Although serological data are useful taxonomic tools for closely related viruses, their interpretation in defining relationships among more distantly related viruses has proven complex (Calisher et al., 1989; Shope, 1995
; Wang et al., 1995
). More recently, the extent of sequence similarity within a given gene has largely been used for species demarcation in each genus of the Rhabdoviridae. In the Lyssavirus genus, for instance, percentage sequence similarity within the nucleoprotein gene has been used for the definition of different virus genotypes (Arai et al., 2003
; Bourhy et al., 1993
; Kuzmin et al., 2003
), and the same methodology has been used for the delineation of different species among the vesiculoviruses and ephemeroviruses (Barr et al., 1991
; Crysler et al., 1990
; Masters & Banerjee, 1987
; Walker et al., 1994
; Wang et al., 1995
).
Our phylogenetic analysis of the 158-residue L polymerase sequence produced an evolutionary tree that generally, although not entirely, conformed to accepted serological groupings and taxa within the Rhabdoviridae (Calisher et al., 1989; Shope, 1995
; Tordo et al., 2004
). In particular, members of four genera Lyssavirus, Novirhabdovirus, Cytorhabdovirus and Nucleorhabdovirus obtained from a variety of host species, including mammals, fish, arthropods and plants, can be easily distinguished and fall into relatively well-supported clades (Fig. 3
). Although the vesiculoviruses and ephemeroviruses also fell into clear monophyletic groups, they are less well supported by quartet puzzling, and each genus contained some unclassified viruses. Furthermore, Kotonkon virus, which causes clinical ephemeral fever in cattle (Kemp et al., 1973
; Tomori et al., 1974
), but which has previously been classified as a lyssavirus, very clearly clustered with members of the genus Ephemerovirus. Lastly, there is some evidence that the two groups of plant rhabdoviruses the cytorhabdoviruses and nucleorhabdoviruses form a distinct clade, although this has relatively low quartet puzzling support. Taastrup virus, which was unassigned (Bock et al., 2004
), is related to cytorhabdoviruses.
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Perhaps the most notable result from our phylogenetic analysis was the strong support (98 %) for a virus supergroup, herein named dimarhabdovirus' (sigla for dipteran-mammal associated rhabdovirus). This contained the four new groups of viruses described above, as well as the Vesiculovirus and Ephemerovirus genera. Despite major differences in genome organization, ephemeroviruses and vesiculoviruses share many similar biological characteristics. They are, together with the other dimarhabdoviruses, the only recognized rhabdovirus genera with viruses that replicate in both vertebrate and invertebrate hosts, and have biological cycles involving transmission by hematophagous dipterans. Although there is strong phylogenetic support for the dimarhabdovirus supergroup, the precise branching order within this group cannot be resolved on the L polymerase data. Indeed, there is a clear need for further phylogenetic studies within the dimarhabdovirus supergroup, particularly with respect to the demarcation of genera, which currently seems to be influenced more by genome structure than hostvector relationships. For example, compared to vesiculoviruses, ephemeroviruses contain multiple additional ORFs, including a second glycoprotein gene (GNS) that appears to have been acquired by gene duplication (Wang & Walker, 1993). There is some evidence that Flanders virus may also have a complex pattern of gene expression (Boyd & Whitaker-Dowling, 1988
). Although the functions of these additional proteins are not understood, revealing the evolution of genome complexity may be an important factor in resolving the taxonomy of this supergroup.
In sum, the sort of molecular phylogenetic analysis undertaken here, especially if combined with data on genome organization, is likely to provide a more useful guide to taxonomic classification, particularly for assignments above the species level and even among all () RNA viruses (Vieth et al., 2004). Indeed, our phylogenetic analysis of a conserved L-gene segment appears to provide a useful taxonomic tool for the rapid classification of rhabdoviruses.
Association between phylogenetic relationships and mode of transmission
A number of important biological conclusions can be drawn from the rhabdovirus phylogeny presented here. First, assuming a mid-point rooting of the tree, there is major split between those viruses that infect fish (novirhabdoviruses) and plants and which employ arthropods as vectors (cytorhabdoviruses and nucleorhabdoviruses), and those viruses that mainly infect mammals, lizards and dipterans (dimarhabdoviruses). Such a division illuminates the biology of a number of key rhabdoviruses. For example, although vesicular stomatitis virus (VSV) is responsible for a disease of horses, cattle and pigs and can be transmitted directly by transcutaneous or transmucosal routes (Stallknecht et al., 1999), there is good evidence that VSV may be an insect virus (Rodriguez, 2002
). Indeed, it has been found to replicate in biting midges (Culicoides) and Simulium blackflies (Mead et al., 1999
), and has been isolated from sandflies, and epidemic and endemic bursts depend on region, season and the presence of dipterans (Lutzomya, Simulidae, Culicoides and Musca domestica) (Gard et al., 1984
; Walker & Cybinski, 1989
). All these factors suggest that VSV may be insect-borne. Similarly, Bovine ephemeral fever virus, which is frequently found in Australasia, Asia and Africa, is also dipteran-transmitted, using vectors such as biting midges and culicine and anopheline mosquitos. Finally, viruses assigned by our phylogenetic analysis to the four new groups (the Le Dantec, Tibrogargan, Hart Park and Almpiwar groups) were all found to infect dipterans and in some cases mammals (Tibrogargan, Le Dantec and Ngaingan viruses) and lizards (Charleville virus) also.
Importantly, there is as yet no evidence for a virus that would constitute a link between plant and fish viruses and dimarhabdoviruses and the lyssaviruses. Furthermore, the uncertainty over branching order at the root of the tree makes it difficult to determine whether the ancestral mode of transmission in the rhabdoviruses was vector or non-vector transmission. A similar lack of resolution at the base of tree was found in a previous phylogenetic analysis of six genera of rhabdoviruses (Vieth et al., 2004). However, the major phylogenetic division between these groups indicates that the biology of the rhabdoviruses could be strongly influenced by mode of transmission and by the host (plant, fish or mammal) and vector (orthopteran, homopteran or dipteran) species. Similar findings have been reported in other RNA viruses, such as the flaviviruses (Gaunt et al., 2001
) and the tick-borne nairoviruses (Honig et al., 2004
).
Finally, it is noteworthy that levels of genetic diversity vary substantially among genera. This is most apparent when comparing the tightly clustered lyssaviruses (the different genotypes of which our phylogenetic analysis cannot easily distinguish) with the cytorhabdoviruses and nucleorhabdoviruses, which are highly diverse. Indeed, the entire Lyssavirus genus, although clearly separate from the other rhabdoviruses, is less divergent than two serotypes (Indiana and New Jersey) of VSV. The most likely explanation for such differences is that these genera differ substantially in age, with the lyssaviruses evolving most recently. However, it is also possible that strong selective constraints acting against sequence change in the lyssaviruses also serve to limit amino acid variation (Guyatt et al., 2003; Holmes et al., 2002
; Kissi et al., 1999
).
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ACKNOWLEDGEMENTS |
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Received 22 April 2005;
accepted 12 July 2005.
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