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Evidence That a Plant Virus Switched Hosts to Infect a Vertebrate and Then Recombined with a Vertebrate-Infecting Virus

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Evidence That a Plant Virus Switched Hosts to Infect a Vertebrate and Then Recombined with a Vertebrate-Infecting Virus Proc. Natl. Acad. Sci. USA Vol. 96, pp. 8022–8027, July 1999 Evolution Evidence that a plant virus switched hosts to infect a vertebrate and then recombined with a vertebrate-infecting virus MARK J. GIBBS* AND GEORG F. WEILLER Bioinformatics, Research School of Biological Sciences, The Australian National University, G.P.O. Box 475, Canberra 2601, Australia Communicated by Bryan D. Harrison, Scottish Crop Research Institute, Dundee, United Kingdom, April 28, 1999 (received for review December 22, 1998) ABSTRACT There are several similarities between the The history of viruses is further complicated by interspecies small, circular, single-stranded-DNA genomes of circoviruses recombination. Distinct viruses have recombined with each that infect vertebrates and the nanoviruses that infect plants. other, producing viruses with new combinations of genes (6, 7); We analyzed circovirus and nanovirus replication initiator viruses have also captured genes from their hosts (8, 9). These protein (Rep) sequences and confirmed that an N-terminal interspecies recombinational events join sequences with dif- region in circovirus Reps is similar to an equivalent region in ferent evolutionary histories; hence, it is important to test viral nanovirus Reps. However, we found that the remaining C- sequence datasets for evidence of recombination before phy- terminal region is related to an RNA-binding protein (protein logenetic trees are inferred. If a set of aligned sequences 2C), encoded by picorna-like viruses, and we concluded that contains regions with significantly different phylogenetic sig- the sequence encoding this region of Rep was acquired from nals and the regions are not delineated, errors may result. one of these single-stranded RNA viruses, probably a calici- Interspecies recombination between viruses has been linked virus, by recombination. This is clear evidence that a DNA to severe disease outbreaks (10), and some analyses suggest that it may be linked to host-switching (7, 11). Fortunately, virus has incorporated a gene from an RNA virus, and the fact newly generated interspecies recombinants are rarely found, that none of these viruses code for a reverse transcriptase suggesting that few have arisen recently. To date no evidence suggests that another agent with this capacity was involved. has been reported of recombination between viruses that Circoviruses were thought to be a sister-group of nanoviruses, infect hosts from different kingdoms, e.g., no evidence of but our phylogenetic analyses, which take account of the vertebrate-infecting viruses recombining with plant-infecting recombination, indicate that circoviruses evolved from a viruses. Furthermore, although evidence has been reported of nanovirus. A nanovirus DNA was transferred from a plant to recombination between RNA viruses (6, 7), and between DNA a vertebrate. This transferred DNA included the viral origin viruses (10, 13), only one report has suggested recombination of replication; the sequence conservation clearly indicates that between an RNA virus and a DNA virus. A glycoprotein gene it maintained the ability to replicate. In view of these prop- appears to have been transferred between a baculovirus and a erties, we conclude that the transferred DNA was a kind of Thogoto-like virus, but the direction of transfer is unclear and virus and the transfer was a host-switch. We speculate that it is possible that both viruses acquired their gene from their this host-switch occurred when a vertebrate was exposed to arthropod hosts independently (12). sap from an infected plant. All characterized caliciviruses The two known circoviruses, Porcine circovirus (PCV) and infect vertebrates, suggesting that the host-switch happened Psittacine beak and feather disease circovirus (BFDV), are first and that the recombination took place in a vertebrate. similar in several ways to a set of plant-infecting viruses previously known as plant circoviruses (14–16), but recently Nanovirus Sometimes viruses are transmitted to a host species that they reclassified in the genus (16, 17). Circoviruses and nanoviruses have small, icosahedral particles, 17–22 nm in have not previously infected or that they rarely infect. Several diameter, and small, circular, single-stranded DNA genomes; of these atypical interspecies transmission events (host- those of circoviruses are about 2 kb long, whereas nanovirus switching events) have led to disease outbreaks in this century genomes are about 1 kb long. The two kinds of virus encode (1–3). Analyses of viral genomic sequences provide a historical a replication initiator protein (Rep), and there are clear perspective on these events; the phylogenies of families of similarities between the sequences of these proteins (14). Reps viruses inferred from sequences often do not match those of initiate rolling circle replication at a nonanucleotide sequence their hosts (2–4), suggesting that there have been many within a longer origin-of-replication sequence (15, 18, 19), and host-switching events in the past. Almost all of these events the nonanucleotide sequences of circoviruses match those of involved the transfer of viruses between hosts in the same some nanoviruses. Two recent phylogenetic analyses placed phylum or division. However, similarities between the ge- Rep sequences of circoviruses and nanoviruses in separate nomes of some plant-infecting, vertebrate-infecting, inverte- groups (15, 17). Here we show that these results may have been brate-infecting, and microbe-infecting viruses indicate that distorted by an interspecies recombinational event and that the they have common ancestors (5), and suggest that at some true evolutionary history of circoviruses and nanoviruses point, ancestral viruses switched between these very different reveals significant information about a major host-switching kinds of hosts. These more radical changes in host preference event. have led to the evolution of many new virus species. They are significant in terms of both disease and evolution; beyond that, Evidence of Interspecies Recombination little about them is known: neither the identity of the original hosts, nor the possibility of linkage between the change in host The nonredundant amino acid sequence database was preference and a specific genetic change. searched by using the program BLASTP, version 2 (20). Initial The publication costs of this article were defrayed in part by page charge Abbreviations: BFDV, Psittacine beak and feather disease circovirus; PCV, Porcine circovirus; P-loop, phosphate-binding loop; Rep, repli- payment. This article must therefore be hereby marked ‘‘advertisement’’ in cation initiator protein. accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. e-mail: mgibbs@ PNAS is available online at www.pnas.org. rsbs.anu.edu.au. 8022 Downloaded by guest on September 30, 2021 Evolution: Gibbs and Weiller Proc. Natl. Acad. Sci. USA 96 (1999) 8023 searches with nanovirus Rep sequences suggested that these circovirus Rep sequences, but we had doubts about the sequences were similar only to Rep sequences of circoviruses relationship because the highest of these scores was only 5.9. and other nanoviruses, but a search with a circovirus Rep For this reason, we repeated the tests using Rep sequences sequence yielded significant similarities with sequences from from which N-terminal sequences, including the P-loop se- caliciviruses and other picorna-like viruses. Picorna-like vi- quence, had been deleted. ruses code for a polyprotein that is cleaved proteolytically to Tests with circovirus sequences that had been truncated up produce an RNA-binding protein known as the 2C-protein to and including the GKT͞S motif confirmed that the simi- (21), and it was the conserved region within the 2C-protein larities were not due solely to the presence of the P-loop, (22) that matched a C-terminal part of the circovirus Rep. because they yielded Z scores as high as 8.6 in comparisons Alignments between circovirus Rep sequences and calicivirus with calicivirus sequences. Tests with circovirus Rep se- 2C-protein sequences yielded Expect values (E values; ref. 20) quences that had been truncated to a point 15 residues to the as small as 4 ϫ 10Ϫ6, and alignments between circovirus and N-terminal side of the GKT͞S motif yielded Z scores as high nanovirus Rep sequences yielded E values as small as 8 ϫ as 9.3 in comparisons with calicivirus sequences and as high as 10Ϫ17. 7.3 in comparisons with sequences from other picorna-like E values Ͻ1 ϫ 10Ϫ2 probably indicate relatedness (20), viruses. Thus, the tests confirmed the common ancestry of the unless they are affected by unusual sequence composition. circovirus Rep and picorna-like virus 2C-proteins. However, concern arose because both the Rep and 2C- The homology of the circovirus and nanovirus Reps was proteins include a short glycine-rich sequence, ending with a similarly confirmed; we used Rep sequences from which Gly-Lys-Thr or a Gly-Lys-Ser (GKT͞S) motif and forming a C-terminal sequences had been deleted, and obtained Z scores phosphate-binding loop (P-loop); this sequence was included up to 10.1. The highest Z score was 2.9 from a pair-wise in the alignment identified by BLASTP. Several kinds of nucle- comparison between a complete nanovirus Rep sequence and otide-binding protein include a P-loop; structural studies show a 2C-protein sequence, 4.6 from a comparison between a some of them to be unrelated (23). Therefore, the presence of 2C-protein sequence and a nanovirus C-terminal Rep se- the P-loop in both 2C-proteins and circovirus Reps could quence, and 3.2 from a comparison between circovirus and result from convergence and this could partly explain their nanovirus C-terminal Rep sequences. However, most of the affinities. To confirm that the various similarities to circovirus comparisons in these three sets yielded scores approaching Reps resulted from common ancestry, rather than similar zero, suggesting that these polypeptides are unrelated or are compositions, we used the program ALIGN (24). This program only very distantly related.
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