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Journal of Virology, January 1999, p. 533-552, Vol. 73, No. 1
Plum Island Animal Disease Center,
Agricultural Research Service, U.S. Department of Agriculture,
Greenport, New York 11944
Received 3 August 1998/Accepted 25 September 1998
The family Poxviridae contains two subfamilies: the
Entomopoxvirinae (poxviruses of insects) and the
Chordopoxvirinae (poxviruses of vertebrates). Here we
present the first characterization of the genome of an
entomopoxvirus (EPV) which infects the North American migratory
grasshopper Melanoplus sanguinipes and other important
orthopteran pests. The 236-kbp M. sanguinipes EPV (MsEPV) genome consists of a central coding region bounded by 7-kbp inverted terminal repeats and contains 267 open reading frames (ORFs), of which
107 exhibit similarity to previously described genes. The presence of
genes not previously described in poxviruses, and in some cases in any
other known virus, suggests significant viral adaptation to the
arthropod host and the external environment. Genes predicting
interactions with host cellular mechanisms include homologues of the
inhibitor of apoptosis protein, stress response protein phosphatase 2C,
extracellular matrixin metalloproteases, ubiquitin, calcium binding
EF-hand protein, glycosyltransferase, and a triacylglyceride lipase.
MsEPV genes with putative functions in prevention and repair of DNA
damage include a complete base excision repair pathway (uracil DNA
glycosylase, AP endonuclease, DNA polymerase The Poxviridae family
consists of large cytoplasmic double-stranded DNA viruses separated
into two subfamilies: the Entomopoxvirinae (poxviruses of
insects) and the Chordopoxvirinae (poxviruses of vertebrates) (130). The entomopoxvirus (EPV) subfamily is
divided into three genera based primarily on differences in viral host range and virion morphology. Genus A viruses infect coleopterans, genus
B viruses infect lepidopterans and orthopterans, and genus C viruses
infect dipterans (7, 54). Insects are the only known hosts
of EPVs, and observed viral host range is restricted to one or a few
related species (7).
A detailed genetic comparison of the two subfamilies has been limited
by the lack of information on EPV genomics. Restriction endonuclease
analysis and DNA cross-hybridization studies have, however, suggested
large genomic differences between lepidopteran group B EPVs and
chordopoxviruses (ChPVs) (63, 102). Limited gene comparisons
have also shown that at certain loci, lepidopteran EPV gene order is
distinct from that of ChPVs (66, 175) and that the degree of
amino acid similarity between EPV and ChPV enzymatic and structural
proteins is low (6, 66, 175).
EPVs have been studied mainly because they are potential insect
biocontrol agents and expression vectors (7, 41, 180). However, EPV genomic organization and molecular mechanisms of replication, pathogenesis, and host range are largely unknown. Few EPV
genes have been characterized in detail, and additional information on
the viral genome and virus-host interactions is necessary to further
develop and improve these viruses as biocontrol agents (6,
175).
Melanoplus sanguinipes EPV (MsEPV) infects the North
American migratory grasshopper M. sanguinipes, an
agriculturally important insect pest, as well as two related
grasshopper species (M. differentialis and M. packardii), the desert locust (Schistocerca gregaria)
(179), and the African migratory locust (Locusta
migratoria) (82, 108). MsEPV produces a large ellipsoid
virion (250 to 300 nm in length) with a rectangular core. Grasshopper
nymphs are infected by MsEPV after oral ingestion of virus-containing
occlusion bodies. Presumably, the virus infects cells of the midgut
prior to generalization of infection to the major target organ, the fat
body (40, 72). Infection results in a slow and debilitating
disease with high mortality, occurring 25 to 30 days postinfection.
High titers of infectious spheroids, which can number up to 8 × 107 per grasshopper, are evident at 12 to 15 days
postinfection (72, 127, 208).
Here, we present a genomic analysis of MsEPV. These data represent the
first characterization of an EPV genome; further, they define the
genetic core of the Poxviridae.
MsEPV DNA isolation and cloning.
MsEPV genomic viral DNA was
extracted from gradient-purified viral occlusion bodies obtained from
the North American migratory grasshopper, M. sanguinipes, as
previously described (102). Random DNA fragments were
obtained by incomplete enzymatic digestion with Tsp509I
endonuclease (New England Biolabs, Beverly, Mass.). DNA fragments of
1.5 to 2.5 kbp were isolated after separation on agarose gels, cloned
into the dephosphorylated EcoRI site of plasmid pUC19, and
grown in Escherichia coli DH10B cells (GIBCO BRL,
Gaithersburg, Md.). Double-stranded plasmids pUC19 was purified by the
rapid boiling method (162). DNA templates were sequenced from both ends with M13 forward and reverse primers, using dideoxy chain terminator sequencing chemistries (163) and an Applied Biosystems PRISM 377 automated DNA sequencer (Perkin-Elmer, Foster City, Calif.). Applied Biosystems sequence software (version 3.0) was
used for lane tracking and trace extraction. Chromatogram traces were
base called with Phred software (43), which also produced a
quality file containing a predicted probability of error at each base
position. The sequences were assembled with Phrap software
(42), using the quality files and default settings to
produce a consensus sequence. Subsequent manual editing was done with
the Consed sequence editor (56). The final DNA consensus sequence represented on average an eightfold redundancy at each base position.
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
The Genome of Melanoplus
sanguinipes Entomopoxvirus
ABSTRACT
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
, and an
NAD+-dependent DNA ligase), a photoreactivation repair
pathway (cyclobutane pyrimidine dimer photolyase), a LINE-type reverse
transcriptase, and a mutT homologue. The presence of these
specific repair pathways may represent viral adaptation for repair of
environmentally induced DNA damage. The absence of previously described
poxvirus enzymes involved in nucleotide metabolism and the
presence of a novel thymidylate synthase homologue suggest that
MsEPV is heavily reliant on host cell nucleotide pools and the de
novo nucleotide biosynthesis pathway. MsEPV and lepidopteran
genus B EPVs lack genome colinearity and exhibit a low level of amino
acid identity among homologous genes (20 to 59%), perhaps
reflecting a significant evolutionary distance between lepidopteran and
orthopteran viruses. Divergence between MsEPV and the
Chordopoxvirinae is indicated by the presence of only 49 identifiable chordopoxvirus homologues, low-level amino acid identity
among these genes (20 to 48%), and the presence in MsEPV of 43 novel
ORFs in five gene families. Genes common to both poxvirus subfamilies,
which include those encoding enzymes involved in RNA transcription and
modification, DNA replication, protein processing, virion
assembly, and virion structural proteins, define the genetic core of
the Poxviridae.
INTRODUCTION
Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
DNA sequence analysis. Genome DNA composition, structure, repeats, and restriction enzyme patterns were analyzed with the Wisconsin Genetics Computer Group (GCG) programs (33). Open reading frames (ORFs) consisting of more than 60 amino acids, and with a methionine start codon and codon usage consistent with known EPV gene sequences from GenBank were considered to be protein encoding (176, 177). DNA and protein comparisons with entries in genetic databases were performed with FASTA (141) and BLAST programs (2). Multiple sequence alignments were performed with the CLUSTAL (74, 187), GCG Pileup (33), MSA (116), and Macaw (166) computer programs. Motif searches were done against the SBASE release 5 (44) and Prosite release 14 (9) databases. Other protein patterns were determined with the profile scanning programs PROBE (134), GIBBS, ASSET (133), and Hidden Markov Model (37, 38). Prediction of transmembrane domains was accomplished with MEMSAT (84, 85) and TopPred (24) software. Signal peptides were predicted with the program Sigseq (195). Physical descriptions of proteins were obtained by using SAPS software (19). Phylogenetic analysis was done with the Phylip computer programs (45) and Phylo_Win graphic tools (51). Gene families were identified by using the following criteria: (i) similarity based on BLAST scores (3) and pairwise clustering with CLUS (94); (ii) cluster profiles produced by PROBE (134); (iii) statistical significance, determined by using PRDF (142); and (iv) the presence of unique motifs, determined by using Pileup, GIBBS, and MACAW (33, 88, 133, 166).
Abbreviations. Organisms have been abbreviated as follows: Amsacta moorei EPV, AmEPV; Autographa californica nuclear polyhedrosis virus, AcNPV; African swine fever virus, ASFV; Choristoneura biennis EPV, CbEPV; Choristoneura fumiferana EPV, CfEPV; cowpox virus, CPV; fowlpox virus, FPV; Heliothis armigera EPV, HaEPV; Melolontha melolontha EPV, MmEPV; Molluscum contagiosum virus, MCV; Orgyia pseudosugata NPV, OpNPV; rabbit fibroma virus, RFV; swinepox virus, SPV; and variola virus, VAR.
Nucleotide sequence accession number. The MsEPV genome sequence has been deposited in GenBank under accession no. AF063866.
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RESULTS AND DISCUSSION |
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Abstract
Introduction
Materials & Methods
Results & Discussion
References
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Organization of the MsEPV genome. The MsEPV genome was assembled into a contiguous sequence of 236,120 bp, similar in size to a previous estimate of 235 kbp (108). Because genomic termini were not sequenced, the left-most nucleotide of the assembled sequence was arbitrarily designated base no. 1.
The nucleotide composition is 81.7% A+T, as previously estimated for MsEPV (101), and is uniformly distributed over the entire length of the MsEPV genome. The total amino acid composition of all MsEPV ORFs reflects a bias for residues with A+T-rich codons. As previously noted in DNAs of other A+T-rich organisms (182), MsEPV preferentially encodes the 6 amino acids specified by codons exclusively composed of A and/or T (Lys, Asn, Ile, Leu, Tyr, and Phe). These amino acids represent the majority (61%) of all those encoded. Two hundred and sixty-seven ORFs defined as methionine-initiated ORFs of greater than 60 amino acids are present (Fig. 1). The high A+T content, which results in a paucity of start codons (2.1%) and a large number of stop codons (14.5%), facilitates ORF identification. Predicted ORFs represent a 99% coding density, with an average ORF length of 854 nucleotides. Forty-four ORFs overlap other ORFs, and 28 smaller ORFs are completely contained within larger ORFs. Only 98 of the 267 MsEPV ORFs have been assigned a putative similarity or function based on homologies with other viral or cellular genes (Tables 1 and 2). Of the 155 most centrally located ORFs (MSV036 to MSV190), 45 (29%) are ChPV homologues. In contrast, of 112 ORFs in the terminal genomic regions (MSV001 to MS035 and MSV191 to MSV267), only 4 (3.5%) are identifiable ChPV homologues (Fig. 1).
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ITRs. Although lacking sequence identity, MsEPV and ChPV ITR tandem repeats are similar (Fig. 1) (121, 190, 204). MsEPV ITRs contain a series of tandemly repeated sequences, 21-bp repeats (27 and 34 copies in the left and right ITRs, respectively) followed by blocks of 7-bp repeats (33 and 32 copies), 69-bp repeats (58 and 52 copies), 26-bp repeats (5 copies each), 72-bp repeats (2 copies each), and a 126-bp repeat (1 copy each). A variable number of incomplete 69-bp repeats (56 to 59 bp) separate the four terminal blocks of repeats. Nucleotide identity within sets of repeats is approximately 60% for the 21-bp repeats and 80 to 98% for the others. Comparison of 4-kbp noncoding ITR regions of vaccinia virus and MsEPV shows that the most numerous repeats, 69 or 70 bp long, are accompanied by less-abundant repeats of 125 to 126 bp and 26 bp and incomplete forms of the 69- to 70-bp repeats (54 to 58 bp). As in orthopoxviruses, there is a nonrepetitive spacer region within each ITR (53, 122). The coding capacity of MsEPV ITRs is limited. Four ORFs are present in the left ITR, and six ORFs are found in the right ITR. Within each ITR, four ORFs are present as single-copy genes. Three copies of the most-terminal ORF are present in the right ITR (MSV265, MSV266, and MSV267).
Gene expression regulatory elements. DNA sequences upstream, within, and downstream of MsEPV ORFs exhibited similarity to promoter and regulatory elements described for other poxviruses, thus suggesting some degree of conservation of gene regulatory mechanisms. Of the 14 MsEPV ORFs with homology to known poxvirus early genes, 8 contain a TGAAAxxxxA motif in the region 5' of the putative translational start codon (Table 1), and an additional four genes contain this motif with only a single nucleotide substitution (data not shown). This putative early-type promoter element resembles the early-promoter core consensus sequence found in other ChPVs (130, 170). This motif has previously been found upstream of the thymidine kinase (TK) genes of other EPVs (58, 119), and a similar motif (TGAATxxxxA) is found upstream of the CbEPV DNA polymerase gene (131). Interestingly, the upstream sequence of the MmEPV fusolin gene, which demonstrates early promoter activity (111), also contains the TGAAAxxxxA motif (52). The vaccinia virus consensus early transcriptional stop sequence (TTTTTxT), which has also been observed downstream of EPV TK and other EPV gene sequences (58, 110, 175, 216), is found within 100 bases of the 3' ends of 49 of the 84 MsEPV ORFs preceded by the TGAAAxxxxA motif.
Twenty-four of 36 MsEPV homologues of late ChPV genes (170) contain the consensus poxvirus-late-promoter sequence (TAAATG) at the translational start site (15, 157, 198). This late-promoter sequence has been previously described for other EPV genes, including those encoding spheroidin, the nucleoside triphosphatase (NTPase) hydrolase I (NPH-I), and topoisomerase (64, 66, 110, 164, 175). Eleven of the 12 remaining putative MsEPV late genes contain upstream sequences that have been found at the start of poxvirus late genes. Such sequences include TAAAT upstream of the translational start site (eight ORFs) (158), TAAAAT (one ORF) (95), and TAATG (three ORFs) (157, 158). Similar to the fusolin genes of other EPVs, 33 MsEPV ORFs contain the TAATG motif at the translational start site (27, 140, 215).Transcription and mRNA biogenesis. MsEPV contains homologues of 18 of the 26 vaccinia virus genes thought to be involved in transcriptional processes (130) (Fig. 1; Table 2). This suggests the presence of conserved mechanisms for generating functional mRNA among the two poxvirus subfamilies. Vaccinia virus RNA polymerase is encoded by at least eight viral genes ranging in size from 7 to 147 kDa. MsEPV homologues of the two largest vaccinia virus subunits, RPO147 (J6R) and RPO132 (A24R), and the smaller subunits RPO35 (A29L), RPO19 (A5R), and RPO18 (D7R) are MSV043, MSV155, MSV149, MSV100, and MSV245, respectively (Table 2). Homologues of the three remaining vaccinia virus RNA polymerase subunits are not identifiable in MsEPV. Amino acid variability within homologous ChPV RPO subunits suggests that other MsEPV subunits may also be highly variable and, thus, undetectable by current computer search and analysis algorithms. In addition, MsEPV contains a homologue (MSV119) of the RNA polymerase-associated protein RAP94 (H4L), which is specifically required for transcription of early-promoter templates (Table 2) (130).
Four homologues of vaccinia virus transcription factors are encoded in MsEPV. MSV113 and MSV063 are homologues of the two subunits of the vaccinia virus early transcription factor, VETFS (D6R) and VETFL (A7L), respectively. MSV187 and MSV065 are homologues of the two late transcription factors VLTF-2 (A1L) and VLTF-3 (A2L) (Table 2). While MSV113 has 44% amino acid identity to vaccinia virus VETFS, the levels of amino acid identity to VETFL, VLTF-2, and VLTF-3 homologues are much lower (22 to 24%). The vaccinia virus late transcription factor VLTF-1 (G8R), VLTF-4 (H5R), and G2R gene product homologues are either absent from the MsEPV genome or unidentifiable. The absence of a VLTF-1 homologue is surprising, since this gene is essential for vaccinia virus replication and is conserved among ChPV genera (130, 170). Four MsEPV ORFs, MSV053, MSV086, MSV113, and MSV148, are homologues of four NTPase-helicase genes found in vaccinia virus (Table 2). These include the NPH-I homologue (D11L), the RNA-DNA helicase (NPH-II) homologue (I8R), the small subunit of the early transcription factor VETFS (D6R), and the DNA helicase (A18R), respectively (Table 2). These MsEPV ORFs contain motifs conserved among the NTPase and helicase enzymes of the RNA and DNA helicase superfamily II (55, 93). Only NPH-I homologues have been previously described in other EPVs (65, 110, 175, 217). As expected, this gene (MSV053) has a higher level of amino acid identity to EPV genes (58%) than to orthopox-, molluscipox-, and leporipoxvirus homologues (33 to 37%). Another ORF (MSV224) also contains carboxy-terminal helicase and NTPase motifs in addition to a cysteine-rich amino terminus, but it lacks homology to other poxvirus genes. MSV148 encodes a homologue of the vaccinia virus A18R gene. A18R encodes a late virion-associated DNA helicase that is essential for correct viral gene expression and productive infection (12, 174). The essential nature of A18R suggests a similar function for MSV148 in MsEPV. MsEPV contains homologues of vaccinia virus genes involved in transcriptional termination, capping, and polyadenylation. MSV067 and MSV124 are homologues of the large and small subunits of the vaccinia virus capping enzyme, D1R and D12L, respectively (Table 2). MSV143 and MSV041 are homologues of the large and small polyadenylation polymerase (PAP) subunits, PAPL (E1L) and PAPS (J3R), respectively (Table 2).Nucleotide metabolism. MsEPV lacks all previously described poxvirus genes involved in nucleotide metabolism (130). Absent are genes encoding TK, thymidylate kinase, the large and small subunits of ribonucleotide reductase, dUTPase, glutaredoxin, and guanylate kinase and the cytidine kinase gene found in FPV (92). The absence of a TK gene in MsEPV is surprising given that TK genes have been identified in other group B EPVs (AmEPV, CbEPV, and CfEPV) (58, 119). This paucity of viral enzymes suggests that MsEPV replication is heavily dependent on host cell nucleotide biosynthesis. These differences in nucleotide metabolism must be of significance for viral cell and/or tissue tropism within the grasshopper host.
Interestingly, and unlike other known poxviruses, MSV238 encodes a thymidylate synthase (TSY) homologue. MSV238 is very similar to TSY genes from eukaryotes (52 to 59% amino acid identity). The 29-amino-acid TSY Prosite motif (PS00091), which contains the catalytic cysteine residue, is also conserved in MSV238 with the exception of a single conservative substitution (leucine to isoleucine) at position 170. Homodimeric TSY catalyzes the methylation of dUMP to the nucleotide precursor dTMP, thus representing an important part of the de novo pathway of pyrimidine biosynthesis (21). Despite its ubiquitous distribution in nature, a viral TSY gene has been observed only in a few herpesviruses and bacteriophages (13, 79, 80).DNA replication. MsEPV contains homologues of most vaccinia virus genes involved in DNA replication, including DNA polymerase (E9L), ATP-GTP binding protein (D5R), DNA topoisomerase (H6R), and replication essential protein kinase (B1R) (Table 2). However, it lacks the processivity factor (A20R) and an ATP-dependent DNA ligase (A50R). Notably, and unlike any other known virus, MsEPV encodes an NAD+-dependent DNA ligase homologue (Table 1).
The MsEPV DNA polymerase (MSV036) is homologous to family B replicative DNA polymerases found in CbEPV (40% identity over 958 amino acids) and other ChPVs (29 to 30% amino acid identity over 900 amino acids). MSV036 also exhibits similarity to the DNA polymerase genes of chlorella virus PBCV-1 (39% identity over 247 amino acids; GenBank accession no. S35209) and ASFV (21% identity over 452 amino acids; GenBank accession no. U27575). MSV036 identity to family B DNA polymerases includes the highly conserved region I, in which the Prosite family signature (PS00116) is 100% conserved (5, 207). MSV089 is homologous to the vaccinia virus ATP-GTP binding protein D5R (29% identity over 560 amino acids). Although more divergent than other ChPV D5R homologues, MSV089 contains regions of similarity throughout the protein, including the extended I (A) type of nucleoside triphosphate binding motif (55). D5R is known to be essential for viral DNA replication and is involved in homologous recombination (159). Like AmEPV, MSV130 encodes a eukaryotic type I DNA topoisomerase with homology to vaccinia virus H6R. In MsEPV, the type I DNA topoisomerase Prosite motif (PS00176) and the active site residue (Tyr-292) are 100% conserved (172). In addition, critical residues required for transesterification by H6R are also conserved (205). Of six critical DNA recognition motifs described in the vaccinia virus protein, three are conserved and two are conservatively substituted in MSV130 (168). MSV162 exhibits similarity to bacterial NAD+-dependent DNA ligases (Fig. 2B). To our knowledge, this is the first NAD+-dependent DNA ligase found in a virus genome. Eukaryotic organisms and other DNA viruses, including all known poxviruses, encode ATP-dependent DNA ligases (26, 67, 89, 103, 115, 213). MSV162 is most similar to bacterial Thermus thermophilus ligase and includes 12 of the 16 Prosite signature residues (PS01055) and the active-site motif Lys-X-Asp-Gly (118). Residues essential for adenylation and deadenylation steps are conserved in MSV162 (Lys-112 and Asp-118, respectively) (118). In addition, MSV162 exhibits partial conservation of a second NAD+-ligase Prosite signature (PS01056) but lacks residues typically conserved in the carboxyl terminus. Given that NAD+-dependent DNA ligases have been found only in bacteria, the presence of this gene in a eukaryotic virus is surprising and suggests that MSV162 has a prokaryotic origin.
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DNA repair.
MsEPV encodes at least seven genes with putative
DNA repair functions (Table 1). These include homologues of genes
encoding a uracil DNA glycosylase (UNG) (MSV208), DNA polymerase (MSV117), AP endonuclease (MSV117), DNA helicase (MSV148), a ChPV
mutT homologue (MSV150), cyclobutane pyrimidine dimer (CPD)
photolyase (MSV235), and a LINE-type reverse transcriptase (RT)
(MSV061). Genes for DNA polymerase and AP endonuclease have
not been previously described in poxviruses. Further, the CPD
photolyase and the LINE-type RT have not been previously found in
any virus genome. The presence of this complement of genes in MsEPV
suggests that virally encoded DNA repair functions are important for
virus survival in nature.
, and DNA ligase act
sequentially through the BER pathway to repair damaged DNA
(30). UNG removes deaminated cytosine (uracil) to generate
apurinic or apyrimidinic sites (AP sites), class II AP endonucleases
remove AP sites after cleaving the DNA strand 5' to the AP site, DNA
polymerase fills the gap by DNA repair synthesis, and DNA ligase
finishes the repair process by closing the gap (20, 30, 124,
203).
MSV208 is most similar to the equine herpesvirus UNG (34% identity
over 214 amino acids); it has significant identity to UNG in bacteria
(Bacillus subtilis PIR accession no. S39712), lower eukaryotes (slime mold [Dictostelium sp.]; GenBank
accession no. U32866), and higher eukaryotes (mouse [Mus
musculus]; GenBank accession no. X99018) (29 to 34% identity
over 195 to 216 amino acids). Surprisingly, MSV208 exhibits much
less similarity to the poxvirus UNG homologues in vaccinia virus
(19% identity over 78 amino acids) and FPV (30% identity over 117 amino acids). The MsEPV gene does, however, contain amino acid
substitutions at the predicted UNG active site. Most notably, an
aspartic acid residue has been replaced by an arginine at the
N-glycosylic bond cleavage site (residue 60 in MSV208). The
significance of these residue changes for protein function is not
known. In vaccinia virus and human cytomegalovirus, UNG enzymes
have been implicated in other functions, including establishing
the correct temporal progression of DNA synthesis and viral replication
(126, 146, 181). Thus, it is possible that MSV208
performs other functions unrelated to BER.
Homologues of both class II AP endonucleases and DNA polymerase are
encoded by MSV117. This gene has homology to eukaryotic and viral class
II AP endonucleases at its amino terminus (amino acids 1 to 296) and
homology to DNA polymerase at its carboxy terminus (amino acids 296 to 607). MSV117 contains most residues of AP endonuclease class II
Prosite signatures 2 and 3 (PS00730 and PS00731, respectively), which
include conserved and potentially metal-binding cysteine and histidine
residues. The degree of identity of MSV117 to eukaryotic and viral DNA
polymerase enzymes is highest at the catalytic region (31%
identity, over 186 amino acids, to rat DNA polymerase (GenBank
accession no. M13961) and includes the DNA polymerase X Prosite
signature (PS00522). Rat DNA polymerase is a smaller protein (335 amino acids) consisting of two domains connected by a
protease-sensitive region (96). The 31-kDa carboxyl-terminal
domain contains the residues critical for catalytic activity as
defined by the crystal structure (29). These residues
are present in MsEPV (Arg-469, Asp-476, and Asp-478). ASFV, another
cytoplasmic DNA virus with an arthropod host, encodes both an AP
endonuclease and a DNA polymerase in separate ORFs (212). The ASFV DNA polymerase (174 amino acids) is the
smallest functional DNA polymerase enzyme that has been described
(137). MSV117 has homology to both ASFV genes.
The fusion of the AP endonuclease and DNA polymerase genes into one
gene has not been previously described. This fusion is reasonable,
however, since the activities of both enzymes are coordinately required
for DNA BER (14). Although a common strategy for RNA viruses
and retroviruses, polyprotein processing has been observed for only a
few vaccinia virus and ASFV structural proteins (4, 130,
173). The absence of vaccinia virus and ASFV proteolytic cleavage
consensus sequences (Ala-Gly/Ala-Ser and Gly-Gly-X, respectively) at the AP endonuclease-DNA polymerase junction in MSV117
suggests that this gene product may have a dual enzymatic function.
A role in DNA repair or recombination is possible for MSV117. DNA
polymerase is the simplest naturally occurring DNA polymerase known, and it is thought to function in a variety of repair mechanisms, including mismatched base repair (203), AP lesion repair
(123), and monofunctional adduct repair (34). DNA
polymerase also seems to be involved in a repair-type DNA synthesis
associated with recombination (68, 77) and with replicative
DNA synthesis (183).
MSV235 shares similarity to class II CPD photolyases from marsupials,
fish, insects, plants, and bacteria (38 to 57% identity over 428 to
445 amino acids) (Fig. 2B). This gene represents the first photolyase
homologue found in a viral genome. CPD photolyase is a photoreactive
enzyme that mediates repair of UV-induced CPDs in DNA (71,
87). The predicted protein of 466 residues exhibits 119 of 141 conserved class II residues (214). Both class II Prosite signatures (PS01083 and PS01084) in the carboxyl-terminal region (residues 298 to 312 and 425 to 444, respectively) are present, except
for a conservative arginine-to-lysine substitution at position 306. Eukaryotic photolyases possess a protruding amino terminus with three
regions of clustered positively charged amino acids which have been
proposed to contain sequences for nuclear or mitochondrial transport
(214). Consistent with a cytoplasmic mode of replication, these regions are absent from MSV235.
The importance of light-dependent DNA repair mechanisms in maintaining
virus populations in nature has recently been demonstrated. Host cell
light-dependent repair mechanisms have been reported to restore
infectivity in up to 52% of sunlight-damaged
viruses in natural marine virus communities (197). The
ubiquity of CPD enzymes in nature (they are found in bacteria, plants,
and mammals), the efficiency of light energy to repair UV-induced DNA
damage, the unienzymatic nature of the system (71), and the
detrimental effects of UV damage on survival of insect DNA viruses
(8) suggest that a photolyase gene might be found in an
insect virus. A virus-encoded photorepair system may thus confer
a selective advantage for MsEPV in nature, where long periods of
environmental exposure may occur.
MSV150 is a homologue of vaccinia virus genes D9R and D10R (Table 2)
(91). All three genes contain the Prosite signature (PS00893) for MutT proteins. The amino acid identity of MSV150 to Shope
fibroma, vaccinia, and molluscum contagiosum virus D10R homologues is
28 to 35% over 87 to 91 residues. MSV150 colinearity to D10R is
interrupted by two regions (amino acids 65 to 117 and 146 to
180) which are absent in the vaccinia virus homologue. Although
the specific function of the vaccinia virus D9R and D10R homologues is unknown (91), bacterial mutT
pyrophosphohydrolase genes help prevent DNA damage and assure fidelity
of RNA transcription within the GO error avoidance system that is
responsible for removing an oxidatively damaged form of guanine
(8-hydroxyguanine or 7,8-dihydro-8-oxoguanine) from both DNA and the
nucleotide pools (125, 184).
MSV061 has significant homology to LINE-type RTs. The seven conserved
regions (domains I to VII) characteristic of diverse retroelements, which include the two critical RT-identifying motifs Asp-h-2X-Ala-Phe and Tyr-h-Asp-Asp-X-3h (where h is any hydrophobic amino acid and X is any amino acid), are also present in MSV061 (Fig.
3) (210). Domains II, III, V,
and VII are perfectly conserved, while domains I, IV, and VI contain
one, two, and one substituted residues, respectively (Fig. 3). Multiple
alignments and phylogenetic trees generated by the
neighbor-joining method with 1,000 bootstrap replicates
(161) show that MSV061 is most closely related (98% bootstrap support) to the LINE-type transposable elements and is
least closely related to RT from yeast introns and E. coli MsDNA (Fig. 3 and data not shown). Other distinctive features of LINE retrotransposons are missing in MSV061, suggesting that it may be the remnant of an old transposition or a truncated LINE. Genes normally adjacent to LINE RTs, such as ORF1 or zinc
finger-containing ORFs, are not found adjacent to MSV061 (46, 152,
209). A triple 21-bp repeat located immediately 3' of the
MSV061 translational stop codon may be the remnant of a transpositional
event. All available data suggest that MSV061 is a functional viral
gene: critical RT motifs are conserved (Fig. 3), the gene shows normal MsEPV base composition with typical MsEPV codon usage (data not shown),
and a potential late promoter (TAATG) is located at the translational start site of the ORF.
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Protein modification. Active participation of MsEPV in protein modification is indicated by the presence of eight viral and cellular gene homologues. These homologues include two protein kinases (MSV154 and MSV173), two type 2C cellular protein phosphatases (MSV081 and MSV135), ubiquitin (MSV144), and three metalloproteases (MSV175, MSV176, and MSV179).
MSV154 and MSV173 are similar to the two vaccinia virion-associated serine/threonine protein kinases, VPK1 (B1R) and VPK2 (F10L), respectively (Table 2). Both ORFs contain the conserved catalytic region IV with an active-site motif of serine/threonine protein kinases (Prosite PS00108), and MSV173 has region I with a protein kinase ATP-binding signature (Prosite PS00107) (69). Although MSV154 lacks the glycine residues that are conserved in the ATP-binding region of other poxvirus and mammalian homologues, it does contain the lysine ATP-binding residue (Prosite PS00107) essential for the kinase activity found in vaccinia virus VPK1 (113). VPK1 is necessary for vaccinia virus DNA replication (151), and VPK2 also appears to be essential for virus viability (112). MSV081 and MSV135 encode protein phosphatase 2C (PP2C) homologues which are similar to each other and to PP2Cs from a broad range of organisms (Fig. 4A). To our knowledge, this is the first report of a PP2C gene in a viral genome. PP2C is the prototypic member of a large family of Mg2+/Mn2+-dependent protein serine/threonine phosphatases (PPM family) present in both eukaryotes and prokaryotes (11). The six invariant metal-coordinating residues common to all PP2C amino-terminal catalytic domains are conserved in MSV081 and MSV135 (Fig. 4A) (11). In addition, MSV081 contains all 8 amino acids present in the PP2C Prosite signature (PS01032) while MSV135 has only a single substitution (Fig. 4A). The different sizes of MSV081 and MSV135 (357 and 239 residues, respectively) indicate that the two are isoforms. MSV081 contains a signal peptide and a cleavage site at the amino terminus, suggesting that it is a secreted protein. Neither ORF contains the 90-amino-acid carboxyl-terminal region characteristic of mammalian PP2Cs (28). Among other functions, PP2C reverses stress-activated protein kinase cascades in the fission yeast (171), inactivates cystic fibrosis transmembrane conductance regulation in humans (189), determines cell fate in bacteria (36), and promotes sex determination in Caenorhabditis elegans (22). Although the pleiotropic functions of this enzyme preclude predictions of specific roles during viral infection, a role in regulation of host intracellular signaling pathways is likely.
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Cellular functions. MSV048 has significant homology to triacylglyceride lipases found in fungi (Rhizopus spp.), eubacteria (Synechocystis spp.), protozoa (Plasmodium spp.), and higher plants (Ipomoea spp.) and similarity at the potential lipase active site of previously described cowpox and ectromelia virus ORFs (196) (Fig. 5D). MSV048 contains a potential catalytic triad (Ser-173, Asp-227, and His-265), the Prosite signature (PS00120), and a high overall degree of amino acid similarity to known lipases (Fig. 5D; Table 1) (18, 31, 32). The predicted size of MSV048 (288 amino acids) is similar to that of most fungal lipases (265 to 297 amino acids), and it exhibits 29% identity over 158 amino acids to the most closely related lipase (from Rhizopus niveous). The presence of a potential signal peptide suggests that the protein is secreted. Given that the grasshopper fat body is the major organ infected by MsEPV (72) and is also the main site of triacylglycerol storage (50, 188), this viral lipase could conceivably be involved in the hydrolysis of lipids, perhaps functioning as a virulence factor.
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85% conservation, and shaded residues
represents amino acids with identity to MsEPV. Amino acid positions are
indicated on the right. (A) Alignment of MSV048 at the active site of
triacylglycerol lipases. Abbreviations: Rhizopus, Rhizopus
niveus, accession no. Structural proteins. Four ChPV virion core protein homologues are present in MsEPV (Table 2). MSV152, MSV164, MSV158, and MSV189 are homologues of vaccinia virus A10L, A3L, L4R, and I7L, which encode the virion core precursor proteins P4a, P4b, and VP8 and the core-associated I7L protein, respectively (130). Interestingly, MSV152 and MSV158, like their vaccinia virus homologues, contain potential proteolytic cleavage sites (104, 192, 193), which suggests that aspects of structural protein processing may be conserved between MsEPV and ChPVs. The proteolysis of P4a, P4b, and VP8 precursor proteins is intimately associated with normal vaccinia virus morphogenesis and production of infectious virions (104, 130, 202).
The overall degree of amino acid similarity between MsEPV and ChPV core protein homologues is low (22 to 28% identity) compared to the similarity observed among ChPV homologues (45 to 65% amino acid identity). Additionally, homologues of the following vaccinia virus structural genes are not found in MsEPV, including A4L core protein, F17L and I3L DNA-binding phosphoproteins, and the G7L, D2L, D3R, and A12L proteins associated with internal parts of intracellular mature virions (130). Of the 14 known membrane proteins in vaccinia virus (130), only L1R is conserved in MsEPV (MSV183), perhaps reflecting the closer relationship between these proteins and host-specific functions. The vaccinia virus L1R gene, which encodes a major myristylated membrane protein that is associated exclusively with the primary membrane surrounding the virion core, is involved in virion assembly (48, 147, 148). Homologues of five genes representing two conserved ChPV gene families are present in MsEPV. Invariant cysteine residues and putative transmembrane domains unique to each family are conserved in these MsEPV ORFs (170). MSV183 and MSV094, homologues of vaccinia virus L1R and F9L, respectively, comprise one gene family. MSV090, MSV121, and MSV142 are homologues of the vaccinia virus genes A16L, G9R, and J5L and comprise the second gene family. Although most of the genes in these two ChPV gene families remain poorly characterized, G9R and A16L have been shown to be myristylated and potentially soluble proteins (120). J5L is thought to be an essential gene (218). The presence of these two gene families in both subfamilies of the Poxviridae suggests that they may provide highly conserved replicative or structural functions. MSV069 is 25 to 28% identical to ChPV rifampin resistance proteins (vaccinia virus D13L) and 54% identical to the HaEPV D13L homologue (139). In vaccinia virus, this essential gene is associated with virion assembly and may direct the formation of Golgi complex-derived viral crescents, which are the first morphologically distinct structures observed during poxvirus assembly (130). Viral crescents have been observed in cells infected with MsEPV and other genus B EPVs (54, 57, 72, 98). Thus, a similar role for MSV069 in EPV morphogenesis is likely. Interestingly, homologues of other vaccinia virus genes associated with early events of virus morphogenesis, such as A14L and A17L (153, 155, 206), were not identified.ChPV homologues of unknown function. MsEPV also encodes homologues of 10 ChPV genes of unknown function (Table 2). Four of these homologues exhibit a high degree of amino acid identity to their ChPV counterparts. MSV237 and vaccinia virus B2R, which exhibit 44% amino acid identity, are located in the right termini of their respective genomes (53). MSV060, which contains a putative signal peptide, and MSV132, which contains a putative amino-terminal transmembrane and signal peptide, exhibit up to 37 and 44% amino acid identity with ChPV homologues of vaccinia virus H2R and A28L, respectively (Table 2). Although MSV115 and vaccinia virus G5R exhibit only 28% amino acid identity, they contain two prominent protein motifs (Asp-Ala-Glu-Phe-X-Met-Cys-2X-Ala and Trp-Pro-4X-Asp-Gln-Asp) which are also conserved in the MCV homologue MC060R.
Gene families of unknown function. MsEPV contains 43 novel ORFs grouped into five gene families. Genes from these families are asymmetrically distributed in regions terminal to the conserved central part of the genome. Family members form tandem arrays occasionally interrupted by other genes (Fig. 1). The lack of similarity between gene family members and known ChPV genes and the presence of host range genes in similar genomic locations in ChPVs suggest that MsEPV gene families perform host range functions. Analysis of sequences upstream of the translational initiation sites suggests that four of the five gene families may be expressed early in infection (Table 1).
The leucine-rich repeat (LRR) family contains 21 ORFs which range in size from 72 to 707 amino acids. The distinguishing feature of this family is a 44-amino-acid repeat that contains regularly spaced leucine residues at 22-amino-acid intervals. A similar motif is present in the AmEPV Q3 ORF (58) and accounts for the homology between LRR family ORFs and the Q3 ORF (Table 1). MsEPV LRR regions are also similar to Listeria internalin proteins (SwissProt accession no. P25146), Trypanosoma adenylate cyclase regulatory protein (SwissProt accession no. P23799), and yeast protein phosphatase SDS22 regulatory protein (SwissProt accession no. P22194). Other known LRR domain-containing proteins participate in protein-protein interactions, and most are involved in signal transduction (90, 109, 136). Seven MsEPV ORFs belong to the alanine-leucine-isoleucine (ALI) motif family. The distinguishing feature of this gene family is an amino-terminal motif which contains invariant alanine, leucine, and isoleucine residues. ORFs containing the ALI motif are divided into two subgroups. Subgroup I includes four ORFs (MSV024, MSV026, MSV196, and MSV204) which range in size from 190 to 222 amino acids and contain Ile-Ile-X-Cys-Phe and Ile-Asp-Leu-Try/Phe-Phe motifs between residues 100 and 150. Subgroup II includes two longer proteins (MSV023 and MSV194) which lack the carboxyl-terminal motifs of the first group and instead contain a different, highly conserved (55% over 365 amino acids) carboxyl terminus. An additional subgroup II ALI motif protein (MSV195) has only 87 amino acids. Both subgroups of ALI family ORFs demonstrated amino-terminal homology to motif regions in putative genes from Chilo iridescent virus (GenBank accession no. AF003534); AcNPV (GenBank accession no. L22858); bacteriophages BK5-T (GenBank accession no. L44593), N15 (GenBank accession no. AF064539), and A2 (GenBank accession no. Y12813); and the bacterium Haemophilus influenzae (GenBank accession no. U32821). While the Chilo iridescent virus ORF showed extensive homology over the length of subgroup I ALI family ORFs, subgroup II ORFs shared an extended amino-terminal motif with the invertebrate virus, bacteriophage, and bacterial ORFs (data not shown). MsEPV ORFs MSV027, MSV029, MSV034, MSV197, MSV205, and MSV252 comprise the tryptophan (W) repeat family. The distinguishing feature of this family is the presence of a repetitive 23-amino-acid motif that contains tryptophan, leucine, and isoleucine residues. These ORFs contain 3 to 12 copies of the motif, with a tryptophan residue spaced every 23 amino acids and a leucine or isoleucine residue spaced every 11 or 12 amino acids. Three of these ORFs (MSV027, MSV197, and MSV205) contain a carboxyl-terminal C3H2C3 (RING-H2) variation of the C3HC4 RING finger motif (17, 165), and one ORF (MSV029) contains a partial RING-H2 motif. The similarity of MsEPV W-repeat ORFs to an uncharacterized 41.6-kDa protein from AcNPV (Table 1) is based primarily on the periodically repeated tryptophan residues present in both proteins. The methionine-threonine-glycine (MTG) family contains four ORFs (MSV021, MSV191, MSV198, and MSV199) and is defined by a 50-amino-acid amino-terminal motif containing these three invariant residues and by an internal motif [SxWxI(5x)FK]. MTG motif ORFs range in size from 158 to 399 amino acid residues. Interestingly, MTG family ORFs demonstrate similarity to ORFs C72R and C74R from Chilo iridescent virus (Table 1). The serine-cysteine-glycine (SCG) family contains five ORFs (MSV214, MSV215, MSV216, MSV217, and MSV062). The distinguishing feature of this family is a 37- to 38-amino-acid motif with invariant serine, cysteine, and glycine residues around position 170 and a predicted transmembrane domain. SCG ORFs are relatively uniform in length (386 to 401 amino acids) and exhibit 34 to 46% amino acid identity.Relationship of MsEPV to other genus B EPVs. MsEPV resembles other EPVs in genome size, DNA composition, and the presence of conserved genes (6, 7). However, the absence of some genes present in other group B EPVs, low levels of amino acid identity to gene homologues, and extensive rearrangements in gene order suggest that MsEPV is distantly related to other described genus B EPVs. Genomic differences among EPVs may reflect the diversity within the hexopod class of arthropods and the long evolutionary presence of insects.
The size of the MsEPV genome (236 kbp) is similar to those reported for AmEPV (225 kbp) and HaEPV (233 kbp) (63, 175), and the high A+T content of MsEPV (82%) is comparable to that of the AmEPV genome (81.5%) (99, 100). ITRs of approximately 7 kbp may also be present in HaEPV (175). MsEPV contains 10 of 16 ORFs previously described in other EPVs. These include the following: AmEPV G1L (vaccinia virus I7L), G2R, G4R (vaccinia virus A28), G5R (spheroidin), and G6L (vaccinia virus NPH-1) (66) and their homologues in CfEPV, CbEPV, and HaEPV (110, 175, 217); CbEPV DNA polymerase (131); AmEPV topoisomerase (143); HaEPV rifampicin resistance protein (vaccinia virus D13L) (139; and the F2 ORF from HaEPV (175). In addition, the 21 ORFs comprising the MsEPV LRR family are similar to the Q3 ORF that is located adjacent to the AmEPV TK gene (58). The LRR gene family and the Q3 ORF contain similar repetitive leucine-rich sequences, and both are located in terminal genomic locations. Known EPV inclusion proteins are divergent or absent in MsEPV. The MsEPV spheroidin protein exhibits only about 20% amino acid identity to spheroidins of genus A (MmEPV) and genus B (HaEPV, AmEPV, and CbEPV) viruses. This contrasts with the 76 to 92% amino acid identity observed among other spheroidins of genus B viruses (6). In addition, MsEPV spheroidin contains approximately one-half (20 residues) the number of cysteines present in AmEPV and CbEPV (10, 215). As might be expected given the lack of observed spindle-shaped inclusions in MsEPV-infected cells (72), MsEPV does not encode a homologue of the major spindle body protein (fusolin, spindolin) that has been identified in group B and group A EPVs (6, 52, 70, 128), nor does it encode a gene with similarity to the AmEPV filament-associated protein (1). MsEPV lacks a TK gene, which is present in AmEPV, CbEPV, and CfEPV (6). The MsEPV genome is not colinear with other described genus B EPV genomes. Of six known genes that are grouped adjacently in the AmEPV genome, MsEPV contains five homologues that are spread over 115 kbp (58, 66). This includes the spheroidin and NPH-I homologues, which despite their juxtaposition in all known genus B EPVs are separated by approximately 20 kbp in MsEPV (66). Similarly, the HaEPV F2L ORF is only 3 kbp from the HaEPV spheroidin gene, while MsEPV homologues of these genes are separated by 70 kbp (175). The MsEPV topoisomerase is adjacent to the vaccinia virus A28L homologue, while in AmEPV these genes are separated by over 100 kbp (143). Thus, the conserved colinear core of genes that has been proposed to exist for EPV genomes (65, 175) may in fact be conserved only among the lepidopteran viruses. Given the above discussion, orthopteran and lepidopteran EPVs may represent two distinct genera of entomopoxviruses.Conclusions. The MsEPV DNA sequence provides the first view of EPV genomics. Comparison of MsEPV with ChPVs establishes the genetic core of the Poxviridae. EPV genome analysis provides basic knowledge of viral functions, including response to DNA damage, nucleotide metabolism, manipulation of cellular stress responses, and virulence, which underlie viral interactions with the arthropod host and the environment. An improved understanding of these interactions will lead to the design of insect biocontrol strategies with enhanced efficacy and versatility.
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ACKNOWLEDGMENTS |
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We thank A. Ciupryk, S. Mireilles, and J. R. Emanuelli for excellent technical assistance; T. Lewis for helpful discussion and assistance; and F. Barany, K. Becker, J. D. Boeke, J. Cox, T. H. Eickbush, A. Gabriel, B. D. Hammock, R. Kretsinger, H. Krokan, S. Parikh, and A. Sancar for comments on EPV gene homologues.
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FOOTNOTES |
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* Corresponding author. Mailing address: Plum Island Animal Disease Center, P.O. Box 848, Greenport, NY 11944-0848. Phone: (516) 323-2500, ext. 330. Fax: (516) 323-2507. E-mail: drock{at}cshore.com.
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REFERENCES |
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Top
Abstract
Introduction
Materials & Methods
Results & Discussion
References
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