Previous Article | Next Article 
Journal of Virology, December 2001, p. 11720-11734, Vol. 75, No. 23
National Center for Biotechnology
Information, National Library of Medicine, National Institutes of
Health, Bethesda, Maryland 20894
Received 29 May 2001/Accepted 7 August 2001
Comparative analysis of the protein sequences encoded in the
genomes of three families of large DNA viruses that replicate, completely or partly, in the cytoplasm of eukaryotic cells (poxviruses, asfarviruses, and iridoviruses) and phycodnaviruses that replicate in
the nucleus reveals 9 genes that are shared by all of these viruses and
22 more genes that are present in at least three of the four compared
viral families. Although orthologous proteins from different viral
families typically show weak sequence similarity, because of which some
of them have not been identified previously, at least five of the
conserved genes appear to be synapomorphies (shared derived characters)
that unite these four viral families, to the exclusion of all other
known viruses and cellular life forms. Cladistic analysis with the
genes shared by at least two viral families as evolutionary characters
supports the monophyly of poxviruses, asfarviruses, iridoviruses, and
phycodnaviruses. The results of genome comparison allow a tentative
reconstruction of the ancestral viral genome and suggest that the
common ancestor of all of these viral families was a nucleocytoplasmic
virus with an icosahedral capsid, which encoded complex systems for DNA
replication and transcription, a redox protein involved in disulfide
bond formation in virion membrane proteins, and probably inhibitors of
apoptosis. The conservation of the disulfide-oxidoreductase, a major
capsid protein, and two virion membrane proteins indicates that the
odd-shaped virions of poxviruses have evolved from the more common
icosahedral virion seen in asfarviruses, iridoviruses, and phycodnaviruses.
The category of virus is biological,
not evolutionary. Viruses are intracellular parasites that
depend on the host cell for their protein synthesis, most of the
reactions of nucleic acid precursor biosynthesis and, to a variable
extent, transcription and replication (15).
Clearly, viruses are not a monophyletic group. There is little doubt,
for example, that small viruses with single-stranded RNA genomes of
only 5 to 10 kb, such as poliovirus or tobacco mosaic virus, on the one
hand, and large viruses with double-stranded DNA (dsDNA) genomes of 100 to 500 kb, such as herpesviruses, poxviruses, or iridoviruses, on the
other hand, have evolved independently. However, comparative analyses
of the genomes of many groups of viruses have suggested common origins for large, heterogeneous assemblages. For example, it appears most
likely that all reverse-transcribing viruses and mobile elements, in
spite of the extreme diversity of their life cycles and the sets of
encoded proteins, have evolved from a common ancestor (17, 56,
70). Even more unexpected evolutionary connections are suggested
by the involvement of homologous enzymes, such as superfamily III
helicases, in genome replication of both RNA and DNA viruses with small
genomes (23), and the central role of the conserved
rolling circle replication initiator protein in single-stranded DNA
(ssDNA) viruses of eukaryotes and bacteria and in bacterial plasmids
(26).
Viruses with large, dsDNA genomes are generally thought to have evolved
by capturing multiple genes from the genomes of cellular organisms,
their hosts. Indeed, many genes of these viruses, particularly those
involved in virus-host interactions, show high levels of protein
sequence similarity to their cellular homologs, which is apparently
indicative of relatively recent acquisition by the viral genomes
(12, 51, 59). However, viruses belonging to a particular
large family, such as the herpesvirus family or the poxvirus family,
share between themselves a core set of genes encoding proteins involved
in DNA replication, transcription, and virion biogenesis, most of which
are only moderately similar to cellular homologs, if such are
detectable at all (3, 51). The existence of core sets of
up to 40 to 50 conserved viral genes (8, 22) establishes
beyond reasonable doubt that the extant members of the families
Herpesviridae and Poxviridae have diverged from
the respective ancestral viruses that already possessed the principal
features of genome replication and expression and of virion structure
that are typical of these viral families. In contrast, it remains
unclear whether there are any evolutionary connections between
different viral families. Poxviruses, African swine fever virus (ASFV,
the archetypal member of the family Asfarviridae), and
iridoviruses are the three families of eukaryotic viruses with large
dsDNA genomes that undergo their replication cycle either entirely in
the cytoplasm (poxviruses) or start their replication in the nucleus
and complete it in the cytoplasm (20, 22, 38, 40, 63, 67),
as opposed to herpesviruses and baculoviruses, whose DNA replication
and transcription occur exclusively in the nucleus (30,
65). Poxviruses, asfarviruses, and iridoviruses encode their own
transcription machinery, which includes, in each case, several RNA
polymerase subunits and additional transcription factors, and share
several other conserved genes (58, 72). Large DNA viruses
isolated from very diverse algae, the Paramecium bursaria
chlorella virus (PBCV) and the related Ectocarpus
siliculosus virus (ESV), members of the Phycodnaviridae
family, also share several genes with nucleocytoplasmic large DNA
viruses, although genomes of these viruses are transcribed in the
nucleus and, accordingly, they lack genes for RNA polymerase subunits
(41, 61). The four families of large eukaryotic DNA
viruses, Poxviridae, Asfarviridae, Iridoviridae, and Phycodnaviridae, to which we
collectively refer here as nucleocytoplasmic large DNA viruses (NCLDV),
have both common and unique features of genomic DNA and virion
structure. Poxviruses, ASFV, and PBCV have linear DNA genomes with
terminal inverted repeats that form covalently closed hairpins
(40, 67, 75), iridoviruses have circularly permuted linear
genomes (60), and ESV appears to have a circular genome
(41). The virions of ASFV, iridoviruses, and PBCV consist
of a DNA-protein core that is surrounded by a lipid bilayer, which in
turn is encased in one or more icosahedral capsid shells (58, 63,
66). Poxviruses have a more complex, unique virion structure,
with a core surrounded by a "brick-shaped" proteolipid shell
(40).
It remains uncertain whether the similarities between the gene
repertoires, genome structures, and virion architectures of different
families of NCLDV are due to independent recruitment of the same or
related host genes driven by the common functional requirements for the
viral replication cycles or by origin from a common viral ancestor.
This crucial dilemma is not readily amenable to conventional
phylogenetic analysis because even homologous proteins of viruses from
different families show moderate or weak sequence conservation and may
be less similar to each other than to the corresponding cellular
homologs (51). At face value, these observations appear to
favor the polyphyletic origin of different viral families. However,
this aspect of the relationships between viruses needs to be
interpreted with caution given the realistic possibility of rapid
evolution of viral genes (44). Moreover, such rapid
divergence potentially might even preclude the very detection of
evolutionary relationships between some viral genes. Given these
considerations, we were interested in delineating the complete set of
conserved genes among NCLDV by applying the most advanced available
methods for sequence similarity detection and assessing the hypothesis
of independent recruitment of similar sets of genes from the host as
opposed to an origin of several viral families from a single, ancestor
virus. We expand the list of conserved genes shared by all or a
majority of NCLDV families and show that origin from a common viral
ancestor is the most parsimonious scenario for the evolution of all of
these viruses.
Viral genome and protein sequences.
Nucleotide sequences of
the complete genomes of large DNA viruses and the corresponding,
predicted protein sequences were extracted from the Genomes division of
the Entrez system (National Center for Biotechnology Information,
National Institutes of Health, Bethesda, Md.
[http://www.ncbi.nlm.nih.gov:80/entrez/query.fcgi?db=Genome]). The complete genomes included in this analysis were from the
following viruses: poxviruses, including vaccinia virus, strain
Copenhagen (VV [21]), variola virus, strain India (VAR
[37]), Molluscum contagiosum virus type 1 (MCV [50]), Shope fibroma virus (SFV [66]), Fowlpox virus (FPV [2]),
Melanoplus sanguinipes entomopoxvirus (MSV
[1]), Amsacta moorei entomopoxvirus (AMV
[8]); asfarviruses, including ASFV (72); iridoviruses,
including fish lymphocystis disease virus (FLDV [58]),
Chilo iridescent virus (CIV [27]); and phycodnaviruses,
including PBCV (type 1 [35]) and ESV (type 1; N. Delaroque, G. Bothe, T. Pohl, R. Knippers, D. G. Mueller, and W. Boland [GenBank NC002687]).
Sequence analysis.
Protein sequences were compared to
protein sequence databases by using the BLASTP program and to
nucleotide sequence databases translated in six frames by using the
TBLASTN program (5). Additional searches for detecting
subtle similarities were performed by using the PSI-BLAST program with
varied cutoffs for including sequences into profiles (4,
5). Multiple alignments of protein sequences were constructed by
using the ClustalW (57) and T_coffee programs
(43), with subsequent manual refinement on the basis of
the PSI-BLAST search results. Protein secondary structure was predicted
by using the PHD program, with a multiple alignment submitted as the
query (47). Protein sequence-structure threading was
performed by using the hybrid fold recognition method
(16).
Identification of clusters of orthologous viral proteins.
In
order to identify sets of orthologous viral proteins, single-linkage
clustering based on BLASTP search results was performed by using the
BLASTCLUST program and an empirically determined alignment score cutoff
of 0.2 bits/position (I. Dondoshansky, Y. I. Wolf, and E. V. Koonin, unpublished data; ftp://ftp.ncbi.nlm.nih.gov/blast). For
resulting clusters that included representatives of two or more viral
families, additional PSI-BLAST searches were performed against the NR
database, with all sequences from the original cluster used as queries.
Position-specific weight matrices obtained through these searches were
saved and used for a second round of searching the NCLDV protein
sequences. This was done to detect potential members of the given
protein cluster encoded in the genomes from other virus families that
could have been missed at the first stage due to low sequence conservation.
Cladistic analysis.
Cladistic analysis was performed by
using the PAUP* version 4.0 package (55). A maximum of
four states, namely, the primitive state (0) and up to three derived
states (1, 2, and 3), were considered. The relationship between the
derived states was assumed to be unordered, that is, a primitive
character could make the transition to any of the derived states if
more than one derived state existed for the given character. Gain of a
novel protein, domain, or sequence motif was scored as a derived
character with respect to its complete absence, which was defined as
the primitive state. The size ranges and domain architectures of
proteins were also used as characters scored in the matrix. The
shortest trees were determined by using the Branch and Bound and the
Exhaustive Search algorithms. The consensus of the shortest trees was
obtained by using the Consensus Tree routine of PAUP. The character
state transitions for each node of the shortest trees were derived by
using the Show Apomorphy routine of PAUP, and this was used to
determine the synapomorphies supporting a given clade.
Clusters of orthologous viral proteins.
Viral proteins tend to
evolve faster than their cellular counterparts, which makes it
difficult to detect homologous relationships for some of them.
Therefore, the detection of orthologous sets of viral proteins is not a
trivial task and, in some cases, requires application of the most
advanced sequence analysis methods. Furthermore, for detecting clusters
of viral orthologs, it was important to compare viral proteins among
themselves only, to limit the search space and thus increase the
sensitivity. Once the clusters were identified, their relationships
with non-NCLDV proteins were investigated by additional sequence
comparisons; the results of these comparisons were then used for
refinement of the NCLDV clusters.
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.23.11720-11734.2001
Common Origin of Four Diverse Families of Large
Eukaryotic DNA Viruses
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
RESULTS AND DISCUSSION
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
TABLE 1.
Distribution of conserved genes in large, cytoplasmic DNA
viruses and Phycodnaviridae
D5 NTPase and helicase.
VV D5R protein is an NTPase that is
essential for viral DNA replication (14). The D5R protein
and its orthologs in other NCLDV are peripheral members of the AAA+
class of NTPases (42), as demonstrated by the detection of
these sequences in iterative database searches started with many AAA+
NTPase sequences. Within the AAA+ class, the D5R family belongs to the
so-called helicase superfamily III (SFIII), which consists
entirely of viral and plasmid proteins (Fig.
1A). Originally, SFIII has been
identified as an assemblage of
(predicted) helicases encoded by small RNA and DNA viruses (23,
31). We found that, in PSI-BLAST searches seeded with the
sequence of the predicted ATPase domains of poxvirus D5R proteins,
statistically significant similarity to E1 proteins of papillomaviruses
(bona fide members of SFIII) was detected in the fifth iteration. The
closest homologs of the predicted NCLDV helicases are encoded by
certain bacteriophages, in some cases integrated into bacterial
chromosomes (Fig. 1A). The predicted helicases of NCLDV and this subset
of bacteriophage helicases share a distinct, conserved region upstream
of the ATPase domain that is not found in any other proteins (Fig. 1A).
The NCLDV group also has several unique motifs within the predicted
ATPase domain (Fig. 1A).
|
3. For example, ASFV C962R was recovered with an
E-value of 10
-helix. The
abbreviations for the NCLDV are defined in Materials and Methods.
Additional abbreviations: AAV, adeno-associated virus 5; AcNPV,
Autographa californica nucleopolyhedrovirus; Bf,
Bacteroides fragilis, Ce, Caenorhabditis
elegans; Cglu, Corynebacterium glutamicum; Cpf,
Clostridium perfringens; Dm, Drosophila
melanogaster; DpAV4, Diadromus pulchellus
ascovirus; Ec, Escherichia coli; HPV08, human
papillomavirus type 8; Hs, Homo sapiens; LcbA2,
Lactobacillus casei bacteriophage A2; Mace,
Methanosarcina acetivorans; MStV, maize streak virus;
phi-105, Bacteriophage phi-105; phiC31, Bacteriophage phiC31; Polio,
human poliovirus 1; SacV, Spodoptera exigua ascovirus;
Si, Sulfolobus islandicus; SV40, Simian virus 40;
Xf, Xylella fastidiosa.
Packaging ATPase A32L. The A32L gene product has been predicted to possess ATPase activity, primarily on the basis of the conservation of the P-loop and Mg2+-binding motifs (33), and subsequently has been shown to be involved in DNA packaging into virions (13). Comparisons of the NCLDV protein sets and iterative database searches detected apparent orthologs of A32L in all NCLDV (Fig. 1B). Although these predicted ATPases may be distantly related to the AAA+ superclass, they showed no specific relationship with any other ATPase family. In particular, other ATPases do not contain readily detectable counterparts of the C-terminal motifs of A32L, which should be considered a synapomorphy of NCLDV (Fig. 1B).
Transcription factor A1L. A1L is a small protein that contains a Zn-finger-domain that we designated the FCS-finger (so named after a characteristic amino acid signature) and functions as a transcriptional transactivator of late VV genes (28); A1L orthologs were found in all NCLDV. The FCS-finger is a previously undetected Zn-binding domain that we identified in several eukaryotic chromatin proteins such as the Drosophila Sex Combs on Middle Leg, Polyhomeotic, Lethal 3 of Malignant Brain Tumor, and vertebrate FIM. This domain is also found fused to the C termini of recombinases from certain prokaryotic transposons. However, A1L orthologs from NCLDV are a distinct stand-alone form of the FCS domain and thus should be considered an NCLDV synapomorphy (Fig. 1C).
Capsid protein D13L.
The virions of different NCLDV have
dramatically different structures. The major capsid proteins of
iridoviruses and phycodnaviruses, both of which have icosahedral
capsids surrounding an inner lipid membrane, showed a high level of
sequence conservation. A more limited, but statistically significant
sequence similarity was observed between these proteins and the major
capsid protein (p72) of ASFV, which also has an icosahedral capsid. It
was surprising, however, to find that all of these proteins shared a
conserved domain with the poxvirus protein D13L, which is an integral
virion component thought to form a scaffold for the formation of viral crescents and immature virions (54). In spite of low
sequence similarity, D13L sequences share a common domain with
conserved predicted structural elements with the major capsid proteins
of the other NCLDV (Fig. 1D). The capsid proteins of iridoviruses, phycodnaviruses, and ASFV have an additional C-terminal domain that is
predicted to adopt the jelly roll fold typical of capsid proteins of
numerous DNA and RNA viruses (46). In poxvirus D13L proteins, the jelly roll domain is replaced by a distinct
-strand-rich domain that showed no detectable relationship with any
known domains. This difference in the C-terminal domains of poxvirus
D13L proteins compared to the major capsid proteins of other NCLDV
probably reflects the new function of D13L as a scaffold for viral crescents.
Virion membrane protein L1R/F9L. Paralogous poxvirus genes L1R and F9L encode membrane proteins that have a conserved domain architecture, with a single, C-terminal transmembrane helix, and an N-terminal, multiple-disulfide-bonded domain (51). The L1R protein is myristoylated and has been implicated in virion assembly (45, 68). Homologs of the L1R/F9L family proteins so far have not been detected outside poxviruses. However, our comparisons revealed apparent representatives of this family in all NCLDV, with the single exception of ESV (Fig. 1E). With the exception of PBCV, all NCLDV share two of the disulfide-bond-forming cysteine residues and have a transmembrane helix C-terminal to the core domain. The PBCV protein is highly divergent and seems to have lost the disulfide-bonding cysteines; however, it has an additional cysteine-rich, EGF-like domain that is also found in other PBCV proteins (data not shown). This domain is inserted between the core L1R-like domain and the C-terminal transmembrane helix.
A conserved structural role for this protein is compatible with the existence of a lipid membrane in all NCLDV, in spite of the major differences in virion structure. Furthermore, the conservation of the myristoylated, disulfide-bonded protein in most of the NCLDV correlates with the conservation of the thiol-disulfide oxidoreductase E10R which, in VV, is required for the formation of disulfide bonds in L1R and F9L (52).Other apparent synapomorphies of NCLDV. Even when apparent orthologs of a viral protein are present in cellular life forms, the viral version may have unique features. An example is the thiol-disulfide oxidoreductase E10R. The proteins of this family encoded by different NCLDV show limited sequence similarity to each other, and some are more similar to apparent orthologs from eukaryotes, such as the yeast ERV1/2 proteins (52). However, all nonviral members of this family share two pairs of conserved cysteines, whereas only one pair is conserved in the proteins from NCLDV.
Another notable ancestral protein family of NCLDV consists of homologs of proliferating cell nuclear antigen (PCNA), a protein that is ubiquitous in cellular life forms and functions as the sliding clamp during DNA replication (11). The members of the PCNA superfamily identified in NCLDV show limited sequence similarity to the cellular homologs; in fact, the poxvirus PCNA homologs (G8R) were identified in this study only through the use of the sequence-structure threading technique. Phylogenetic analyses on the PCNA superfamily indicated that the NCLDV PCNA homologs tend to cluster together, to the exclusion of eukaryotic homologs, but typically form longer branches than any cellular PCNAs, suggesting rapid divergence during NCLDV evolution (unpublished data). Poxvirus G8R is the most divergent member of the PCNA superfamily. The available experimental evidence points to a principal role of this protein in vaccinia virus late gene transcription, rather than replication (69, 74), suggesting a causal connection between rapid sequence divergence and the change of function. Among the proteins that are conserved in three of the four NCLDV families, the most notable one is the membrane protein that, in poxviruses, is represented by three paralogs, J5L, G9R, and A16L, which are predicted to form multiple disulfide bonds (51). These proteins resemble the virion membrane proteins of the L1R/F9L group in domain architecture, but appear not to be homologous to them or to any other proteins.Cladistic analysis suggests monophyly of NCLDV. Phylogenetic tree analysis of those NCLDV proteins that have homologs in other viruses and in cellular life forms, such as DNA polymerase, helicases and others (Table 1), fails to support monophyly of NCLDV (26; unpublished observations). However, this cannot be considered strong evidence against monophyly because viral genomes tend to evolve rapidly, resulting in distortions of phylogenetic tree topologies. Indeed, as discussed above, even those groups of orthologous NCLDV proteins that comprise clear synapomorphies show only limited sequence conservation. Therefore, as an alternative approach for assessing the evolutionary relationships among the NCLDV, we undertook formal cladistic analysis (25) of viral gene sets after identifying probable orthologs in other viruses and cellular organisms (Table 1). All genes that occur in at least two families of NCLDV were scored as described in Materials and Methods to obtain character states for the terminal taxa under examination. The 11 terminal taxa considered in this analysis were chordopox viruses, entomopox viruses, asfarviruses (ASFV), iridoviruses (CIV and FLDV), PBCV, ESV, herpesviruses, baculoviruses, bacteriophage T4, and the eukaryotic cell (host cell). A total of 59 characters were scored over these 11 taxa to construct the data matrix used in the cladistic analysis (data not shown [available as supplementary material from the authors]).
Trees that provided the shortest path of character state changes to result in the character configuration observed in the terminal taxa were identified by using the Branch and Bound method and the Exhaustive Search algorithm that evaluates all possible tree topologies for the given terminal taxa. One most parsimonious tree was found that supported the monophyly of the NCLDV by 16 synapomorphies. As expected, the monophyly of the so-called phycodnavirus clade (PBCV plus ESV) and the poxvirus clade (entomopox viruses plus chordopoxviruses) was strongly supported (Fig. 2). In addition, there was a weaker support for the monophyly of the animal viruses (poxviruses plus ASFV plus iridoviruses), to the exclusion of the phycodnaviruses, by six synapomorphies. Furthermore, the tree contained a clade consisting of poxviruses and asfarviruses, to the exclusion of the iridoviruses, which was supported by eight synapomorphies. This tree was used to extract a list of derived shared characters for the NCLDV clade that were used in reconstructing the repertoire of genes present in the hypothetical NCLDV (see below). The monophyly of the three animal viral families, namely, asfarviruses, iridoviruses, and poxviruses, emerged consistently with different sets of characters, but the relationships among these families were highly sensitive to minor changes in characters used in the analysis (data not shown). Thus, the actual branching pattern within the animal NCLDV clade requires additional data for confident resolution.
|
Hypothetical ancestral NCLDV. Given the support for a monophyletic NCLDV clade, the possibility emerges for an approximate reconstruction of the hypothetical ancestral virus. The genes that are shared by all viruses within this clade are obvious candidates for ancestral origin but, additionally, other genes identified as synapomorphies of the NCLDV clade are also, according to the parsimony principle, likely to have been present in their last common ancestor. These typically are genes present in the majority of the NCLDV taxa considered in this analysis. Under this reasoning, the absence of otherwise conserved genes in one lineage is attributed to gene loss, in case of essential genes accompanied by nonorthologous gene displacement (32). Lineage-specific gene loss obviously occurred also within individual NCLDV families, particularly in ESV, which does not have many genes conserved in all or most NCLDV, including PBCV, and, among poxviruses, in MCV that has lost all genes involved in nucleotide metabolism (51). A probable example of displacement is the topoisomerase function that is represented by the predicted ancestral form, type II topoisomerase, in asfarviruses, iridoviruses, and phycodnaviruses (except for ESV, which apparently has lost this gene), whereas poxviruses have an unrelated type IB topoisomerase. Some of the genes that are conserved in only two of the NCLDV families also might be part of the legacy of the ancestral virus, but in these cases, it is difficult to rule out alternative scenarios, such as independent acquisition from the host or horizontal gene transfer.
Under these assumptions, we arrive at a conservative list of 31 ancestral viral genes (Table 1); for comparison, all poxviruses share ca. 50 genes (8). Considering that the ancestral virus might have been a simpler entity than its extant descendants, even this conservative reconstruction may be a reasonable approximation of the ancestral set of essential viral genes. Examination of this list suggests that the ancestral NCLDV already had fairly elaborate systems for genome replication and expression, some enzymes of nucleotide metabolism, a packaging mechanism, capsid and membrane virion proteins, an electron-transfer system for disulfide-bond formation in the latter, a mechanism of protein phosphorylation-dephosphorylation probably involved in the regulation of virion morphogenesis, and possibly an apoptosis inhibitor (Table 2).
|
Relationships between NCLDV and other genetic elements and origin of NCLDV. Many NCLDV genes have homologs or even apparent orthologs in other viruses and plasmids (Table 1). In particular, multiple relationships have been previously noticed to exist between NCLDV genes (specifically, those of poxviruses) and genes of T-even bacteriophages (34, 62). However, neither T-even phages nor herpesviruses or baculoviruses possess a significant subset of the core gene set of the NCLDV (Table 1). Furthermore, the genes that are shared do not show appreciable synapomorphic features. Therefore, direct evolutionary relationships between these classes of viruses apparently cannot be positively established. The observed overlaps between gene sets can be explained largely by independent acquisition of genes that are generically required for DNA virus replication (for example, DNA polymerase, ribonucleotide reductase, or thymidylate kinase) and, possibly, some cases of horizontal gene exchange.
A more coherent relationship appears to exist between the NCLDV and linear DNA plasmids from fungal mitochondria, with five shared genes (of the 10 to 12 genes that are typically present on these plasmids [18, 39]) (Table 1). Importantly, these seem to be the principal genes that are required for DNA virus genome expression in the cytoplasm, including two RNA polymerase subunits, a helicase involved in transcription, and a capping enzyme with a conserved domain architecture (Table 1). In at least one case, that of the D6R-type helicase, the NCLDV proteins show high sequence similarity to the plasmid homolog, to the exclusion of other homologous helicases (data not shown). It seems plausible that the fungal plasmids indeed contain a part of the core gene set of the hypothetical ancestral NCLDV. However, the fungal plasmid genomes have a terminal protein that functions in replication priming and, in this respect, resemble adenoviruses and protein-priming DNA phages (48), rather than NCLDV; the monophyly of DNA polymerases from protein-priming viruses and plasmids is supported by phylogenetic tree analysis (29). Thus, the data suggest complex evolutionary relationships, with components of the replication and expression systems drawn from different types of genetic elements, rather than a direct link between the NCLDV and fungal plasmids. A complex evolutionary scenario for the origin of the NCLDV, including multiple gene exchanges between different types of genomes, is suggested by the phyletic provenance of several other genes shared by all or a subset of NCLDV families. These include the replicative helicase D5R, the Holliday junction resolvase (HJR) A22R, and the predicted protease I7L (Table 1). The distribution of the D5R homologs is particularly unusual. As shown above (Fig. 1), true orthologs of the NCLDV replicative helicase were detected only in certain bacteriophages. More distant members of the helicase III superfamily are encoded by diverse small genetic elements, including ssDNA viruses (geminiviruses and parvoviruses), small dsDNA viruses (papovaviruses), positive-strand RNA viruses (for example, picornaviruses), some phages, and plasmids. So far, no members of this superfamily encoded in genomes of cellular life forms (some prophages notwithstanding) have been detected. This distribution pattern of an essential viral gene suggests a long history of dissemination between (relatively) small genomes, perhaps tracing back to the ancient RNA world. A different evolutionary history appears plausible for the RuvC-like HJR A22R, which is present in poxviruses, at least some iridoviruses, and phycodnaviruses, suggesting that it might have been inherited from the common ancestor of the NCLDV. This enzyme belongs to a family of resolvases that are common in bacteria but not detectable in eukaryotes, except for a nuclease that functions in fungal mitochondria; the latter shows the strongest (albeit limited) sequence similarity to the resolvases of NCLDV (19). This suggests at least two horizontal transfers, from protomitochondria to fungi and from fungi to the ancestral NCLDV (assuming that this resolvase indeed is inherited by NCLDV from their common ancestor). In the lineages which lack the RuvC-like HJR, such as PBCV and ASFV, it might have been displaced by an alternative enzyme, namely, the Lambda-type exonuclease that is present in these viruses (6) (Table 1) or the RecB-like nuclease in PBCV. The available data are insufficient to reconstruct a complete evolutionary scenario for the origin of the ancestral NCLDV. Genome sequencing of representatives of additional viral families has the potential to shed light on the evolutionary source(s) of NCLDV as suggested, for example, by the recent preliminary analysis of the genome of the archaeal virus SIRV1 (9). This virus has a relatively small genome of 32 kB with covalently closed hairpins at the ends, which resembles the genome structure of poxviruses, asfaviruses, and phycodnaviruses. However, the HJR and dUTPase of SIRV1 show clear archaeal affinities, emphasizing a difference from NCLDV (unpublished data). Taken together, the above observations show that the ancestral viral genome probably assembled via gradual accretion of genes from different genetic sources, including host genomes, plasmids, and other viruses. It appears that a complex history of multiple horizontal genes transfers and gene losses both preceded and succeeded the emergence of the ancestral NCLDV. Thus, it is all the more notable that this evolutionary focal point can be identified and some basic aspects of the replication of the ancestral virus can be reconstructed with reasonable confidence on the basis of a detailed comparison of extant viral genomes.| |
ACKNOWLEDGMENTS |
|---|
We thank Bernard Moss for critical reading of the manuscript and useful suggestions and Stewart Shuman for a helpful discussion.
| |
ADDENDUM IN PROOF |
|---|
While this article was being processed for production, a paper describing the sequence of the ESV1 genome was published (N. Delaroque, D. G. Muller, G. Bothe, T. Pohl, R. Knippers, and W. Boland, Virology 287:112-132, 2001).
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bldg. 38A, 8600 Rockville Pike, Bethesda, MD 20894. Phone (310) 435-5913. Fax: (310) 435-7794. E-mail: koonin{at}ncbi.nlm.nih.gov.
| |
REFERENCES |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results and Discussion
References
|
|---|
| 1. |
Afonso, C. L.,
E. R. Tulman,
Z. Lu,
E. Oma,
G. F. Kutish, and D. L. Rock.
1999.
The genome of Melanoplus sanguinipes entomopoxvirus.
J. Virol.
73:533-552 |
| 2. |
Afonso, C. L.,
E. R. Tulman,
Z. Lu,
L. Zsak,
G. F. Kutish, and D. L. Rock.
2000.
The genome of fowlpox virus.
J. Virol.
74:3815-3831 |
| 3. |
Alba, M. M.,
R. Das,
C. A. Orengo, and P. Kellam.
2001.
Genomewide function conservation and phylogeny in the Herpesviridae.
Genome Res.
11:43-54 |
| 4. |
Altschul, S. F., and E. V. Koonin.
1998.
PSI-BLAST a tool for making discoveries in sequence databases.
Trends Biochem. Sci.
23:444-447[CrossRef][Medline].
|
| 5. |
Altschul, S. F.,
T. L. Madden,
A. A. Schaffer,
J. Zhang,
Z. Zhang,
W. Miller, and D. J. Lipman.
1997.
Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
Nucleic Acids Res.
25:3389-3402 |
| 6. |
Aravind, L.,
K. S. Makarova, and E. V. Koonin.
2000.
Holliday junction resolvases and related nucleases: identification of new families, phyletic distribution and evolutionary trajectories.
Nucleic Acids Res.
28:3417-3432 |
| 7. |
Aravind, L.,
D. R. Walker, and E. V. Koonin.
1999.
Conserved domains in DNA repair proteins and evolution of repair systems.
Nucleic Acids Res.
27:1223-1242 |
| 8. | Bawden, A. L., K. J. Glassberg, J. Diggans, R. Shaw, W. Farmerie, and R. W. Moyer. 2000. Complete genomic sequence of the Amsacta moorei entomopoxvirus: analysis and comparison with other poxviruses. Virology 274:120-139[CrossRef][Medline]. |
| 9. | Blum, H., W. Zillig, S. Mallok, H. Domdey, and D. Prangishvili. 2001. The genome of the archaeal virus SIRV1 has features in common with genomes of eukaryal viruses. Virology 281:6-9[CrossRef][Medline]. |
| 10. | Brick, D. J., R. D. Burke, L. Schiff, and C. Upton. 1998. Shope fibroma virus RING finger protein N1R binds DNA and inhibits apoptosis. Virology 249:42-51[CrossRef][Medline]. |
| 11. | Bruck, I., and M. O'Donnell. 2001. The ring-type polymerase sliding clamp family. Genome Biol. 2:3001.1-3001.3. |
| 12. | Bugert, J. J., and G. Darai. 2000. Poxvirus homologues of cellular genes. Virus Genes 21:111-133[CrossRef][Medline]. |
| 13. |
Cassetti, M. C.,
M. Merchlinsky,
E. J. Wolffe,
A. S. Weisberg, and B. Moss.
1998.
DNA packaging mutant: repression of the vaccinia virus A32 gene results in noninfectious, DNA-deficient, spherical, enveloped particles.
J. Virol.
72:5769-5780 |
| 14. | Evans, E., N. Klemperer, R. Ghosh, and P. Traktman. 1995. The vaccinia virus D5 protein, which is required for DNA replication, is a nucleic acid-independent nucleoside triphosphatase. J. Virol. 69:5353-5361[Abstract]. |
| 15. | Fields, B. N. 1996. Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa. |
| 16. | Fischer, D. 2000. Hybrid fold recognition: combining sequence derived properties with evolutionary information. Pac. Symp. Biocomput. 2000:119-130. |
| 17. | Flavell, A. J. 1995. Retroelements, reverse transcriptase and evolution. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 110:3-15[CrossRef][Medline]. |
| 18. | Fukuhara, H. 1995. Linear DNA plasmids of yeasts. FEMS Microbiol. Lett. 131:1-9[CrossRef][Medline]. |
| 19. |
Garcia, A. D.,
L. Aravind,
E. V. Koonin, and B. Moss.
2000.
Bacterial-type DNA Holliday junction resolvases in eukaryotic viruses.
Proc. Natl. Acad. Sci. USA
97:8926-8931 |
| 20. | Garcia-Beato, R., M. L. Salas, E. Vinuela, and J. Salas. 1992. Role of the host cell nucleus in the replication of African swine fever virus. DNA Virol. 188:637-649. |
| 21. | Goebel, S. J., G. P. Johnson, M. E. Perkus, S. W. Davis, J. P. Winslow, and E. Paoletti. 1990. The complete DNA sequence of vaccinia virus. Virology 179:247-266[CrossRef][Medline]; 517-563. |
| 22. |
Goorha, R.
1982.
Frog virus 3 DNA replication occurs in two stages.
J. Virol.
43:519-528 |
| 23. | Gorbalenya, A. E., E. V. Koonin, and Y. I. Wolf. 1990. A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett. 262:145-148[CrossRef][Medline]. |
| 24. | Hannenhalli, S., C. Chappey, E. V. Koonin, and P. A. Pevzner. 1995. Genome sequence comparison and scenarios for gene rearrangements: a test case. Genomics 30:299-311[CrossRef][Medline]. |
| 25. | Harvey, P. H., and M. D. Pagel. 1991. The comparative method in evolutionary biology. Oxford University Press, Oxford, England. |
| 26. |
Ilyina, T. V., and E. V. Koonin.
1992.
Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria.
Nucleic Acids Res.
20:3279-3285 |
| 27. | Jakob, N. J., K. Muller, U. Bahr, and G. Darai. 2001. Analysis of the first complete DNA sequence of an invertebrate iridovirus: coding strategy of the genome of Chilo iridescent virus. Virology 286:182-196[CrossRef][Medline]. |
| 28. |
Keck, J. G.,
G. R. Kovacs, and B. Moss.
1993.
Overexpression, purification, and late transcription factor activity of the 17-kilodalton protein encoded by the vaccinia virus A1L gene.
J. Virol.
67:5740-5748 |
| 29. | Knopf, C. W. 1998. Evolution of viral DNA-dependent DNA polymerases. Virus Genes 16:47-58[CrossRef][Medline]. |
| 30. |
Kool, M.,
C. H. Ahrens,
J. M. Vlak, and G. F. Rohrmann.
1995.
Replication of baculovirus DNA.
J. Gen. Virol.
76:2103-2118 |
| 31. |
Koonin, E. V.
1993.
A common set of conserved motifs in a vast variety of putative nucleic acid-dependent ATPases including MCM proteins involved in the initiation of eukaryotic DNA replication.
Nucleic Acids Res.
21:2541-2547 |
| 32. | Koonin, E. V., A. R. Mushegian, and P. Bork. 1996. Non-orthologous gene displacement. Trends Genet. 12:334-336[Medline]. |
| 33. | Koonin, E. V., T. G. Senkevich, and V. I. Chernos. 1993. Gene A32 product of vaccinia virus may be an ATPase involved in viral DNA packaging as indicated by sequence comparisons with other putative viral ATPases. Virus Genes 7:89-94[CrossRef][Medline]. |
| 34. | Kutter, E., K. Gachechiladze, A. Poglazov, E. Marusich, M. Shneider, P. Aronsson, A. Napuli, D. Porter, and V. Mesyanzhinov. 1995. Evolution of T4-related phages. Virus Genes 11:285-297[CrossRef][Medline]. |
| 35. | Li, Y., Z. Lu, L. Sun, S. Ropp, G. F. Kutish, D. L. Rock, and J. L. Van Etten. 1997. Analysis of 74 kb of DNA located at the right end of the 330-kb chlorella virus PBCV-1 genome. Virology 237:360-377[CrossRef][Medline]. |
| 36. |
Martin, J. P.,
A. M. Aubertin,
L. Tondre, and A. Kirn.
1984.
Fate of frog virus 3 DNA replicated in the nucleus of arginine-deprived CHO cells.
J. Gen. Virol.
65:721-732 |
| 37. | Massung, R. F., J. J. Esposito, L. I. Liu, J. Qi, T. R. Utterback, J. C. Knight, L. Aubin, T. E. Yuran, J. M. Parsons, V. N. Loparev, et al. 1993. Potential virulence determinants in terminal regions of variola smallpox virus genome. Nature 366:748-751[CrossRef][Medline]. |
| 38. | McAuslan, B. R., and R. W. Armentrout. 1974. The biochemistry of icosahedral cytoplasmic deoxyviruses. Curr. Top. Microbiol. Immunol. 68:77-105. |
| 39. | Meinhardt, F., R. Schaffrath, and M. Larsen. 1997. Microbial linear plasmids. Appl. Microbiol. Biotechnol. 47:329-336[CrossRef][Medline]. |
| 40. | Moss, B. 1996. Poxviridae: the viruses and their replication, p. 2637-2671. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa. |
| 41. | Muller, D. G., M. Kapp, and R. Knippers. 1998. Viruses in marine brown algae. Adv. Virus Res. 50:49-67[Medline]. |
| 42. |
Neuwald, A. F.,
L. Aravind,
J. L. Spouge, and E. V. Koonin.
1999.
AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes.
Genome Res.
9:27-43 |
| 43. | Notredame, C., D. G. Higgins, and J. Heringa. 2000. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302:205-217[CrossRef][Medline]. |
| 44. | Pagel, M. 1999. Inferring the historical patterns of biological evolution. Nature 401:877-884[CrossRef][Medline]. |
| 45. |
Ravanello, M. P., and D. E. Hruby.
1994.
Characterization of the vaccinia virus L1R myristylprotein as a component of the intracellular virion envelope.
J. Gen. Virol.
75:1479-1483 |
| 46. | Rossmann, M. G., and J. E. Johnson. 1989. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58:533-573[CrossRef][Medline]. |
| 47. | Rost, B., and C. Sander. 1994. Combining evolutionary information and neural networks to predict protein secondary structure. Proteins 19:55-72[CrossRef][Medline]. |
| 48. | Salas, M. 1991. Protein-priming of DNA replication. Annu. Rev. Biochem. 60:39-71[CrossRef][Medline]. |
| 49. | Schuler, G. D., S. F. Altschul, and D. J. Lipman. 1991. A workbench for multiple alignment construction and analysis. Proteins 9:180-190[CrossRef][Medline]. |
| 50. | Senkevich, T. G., J. J. Bugert, J. R. Sisler, E. V. Koonin, G. Darai, and B. Moss. 1996. Genome sequence of a human tumorigenic poxvirus: prediction of specific host response-evasion genes. Science 273:813-816[Abstract]. |
| 51. | Senkevich, T. G., E. V. Koonin, J. J. Bugert, G. Darai, and B. Moss. 1997. The genome of molluscum contagiosum virus: analysis and comparison with other poxviruses. Virology 233:19-42[CrossRef][Medline]. |
| 52. |
Senkevich, T. G.,
C. L. White,
E. V. Koonin, and B. Moss.
2000.
A viral member of the ERV1/ALR protein family participates in a cytoplasmic pathway of disulfide bond formation.
Proc. Natl. Acad. Sci. USA
97:12068-12073 |
| 53. |
Shors, T.,
J. G. Keck, and B. Moss.
1999.
Down regulation of gene expression by the vaccinia virus D10 protein.
J. Virol.
73:791-796 |
| 54. |
Sodeik, B.,
G. Griffiths,
M. Ericsson,
B. Moss, and R. W. Doms.
1994.
Assembly of vaccinia virus: effects of rifampin on the intracellular distribution of viral protein p65.
J. Virol.
68:1103-1114 |
| 55. | Swofford, D. L. 2000. PAUP*: phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Sunderland, Mass. |
| 56. | Temin, H. M. 1985. Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol. Biol. Evol. 2:455-468[Abstract]. |
| 57. |
Thompson, J. D.,
T. J. Gibson,
F. Plewniak,
F. Jeanmougin, and D. G. Higgins.
1997.
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
Nucleic Acids Res.
25:4876-4882 |
| 58. | Tidona, C. A., and G. Darai. 1997. The complete DNA sequence of lymphocystis disease virus. Virology 230:207-216[CrossRef][Medline]. |
| 59. |
Tidona, C. A., and G. Darai.
2000.
Iridovirus homologues of cellular genesimplications for the molecular evolution of large DNA viruses.
Virus Genes
21:77-81[CrossRef][Medline].
|
| 60. | Tidona, C. A., and G. Darai. 1997. Molecular anatomy of lymphocystis disease virus. Arch. Virol. Suppl. 13:49-56[Medline]. |
| 61. | Van Etten, J. L., and R. H. Meints. 1999. Giant viruses infecting algae. Annu. Rev. Microbiol. 53:447-494[CrossRef][Medline]. |
| 62. |
Villarreal, L. P., and V. R. DeFilippis.
2000.
A hypothesis for DNA viruses as the origin of eukaryotic replication proteins.
J. Virol.
74:7079-7084 |
| 63. | Vinuela, E. 1985. African swine fever virus. Curr. Top. Microbiol. Immunol. 116:151-170[Medline]. |
| 64. | Webster, A., R. T. Hay, and G. Kemp. 1993. The adenovirus protease is activated by a virus-coded disulphide-linked peptide. Cell 72:97-104[CrossRef][Medline]. |
| 65. | Whitley, R. J. 1996. Herpes simplex viruses, p. 2297-2342. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 3rd ed. Lippincott-Raven Publishers, Philadelphia, Pa. |
| 66. | Willer, D. O., G. McFadden, and D. H. Evans. 1999. The complete genome sequence of shope (rabbit) fibroma virus. Virology 264:319-343[CrossRef][Medline]. |
| 67. | Williams, T. 1996. The iridoviruses. Adv. Virus Res. 46:345-412[Medline]. |
| 68. | Wolffe, E. J., S. Vijaya, and B. Moss. 1995. A myristylated membrane protein encoded by the vaccinia virus L1R open reading frame is the target of potent neutralizing monoclonal antibodies. Virology 211:53-63[CrossRef][Medline]. |
| 69. |
Wright, C. F., and A. M. Coroneos.
1993.
Purification of the late transcription system of vaccinia virus: identification of a novel transcription factor.
J. Virol.
67:7264-7270 |
| 70. | Xiong, Y., and T. H. Eickbush. 1990. Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J. 9:3353-3362[Medline]. |
| 71. | Yan, X., N. H. Olson, J. L. Van Etten, M. Bergoin, M. G. Rossmann, and T. S. Baker. 2000. Structure and assembly of large lipid-containing dsDNA viruses. Nat. Struct. Biol. 7:101-103[CrossRef][Medline]. |
| 72. | Yanez, R. J., J. M. Rodriguez, M. L. Nogal, L. Yuste, C. Enriquez, J. F. Rodriguez, and E. Vinuela. 1995. Analysis of the complete nucleotide sequence of African swine fever virus. Virology 208:249-278[CrossRef][Medline]. |
| 73. |
Zemskov, E. A.,
W. Kang, and S. Maeda.
2000.
Evidence for nucleic acid binding ability and nucleosome association of Bombyx mori nucleopolyhedrovirus BRO proteins.
J. Virol.
74:6784-6789 |
| 74. |
Zhang, Y.,
J. G. Keck, and B. Moss.
1992.
Transcription of viral late genes is dependent on expression of the viral intermediate gene G8R in cells infected with an inducible conditional-lethal mutant vaccinia virus.
J. Virol.
66:6470-6479 |
| 75. | Zhang, Y., P. Strasser, R. Grabherr, and J. L. Van Etten. 1994. Hairpin loop structure at the termini of the chlorella virus PBCV-1 genome. Virology 202:1079-1082[CrossRef][Medline]. |
Journal of Virology, December 2001, p. 11720-11734, Vol. 75, No. 23
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.23.11720-11734.2001
This article has been cited by other articles:
-
Bisht, H., Weisberg, A. S., Szajner, P., Moss, B.
(2009). Assembly and Disassembly of the Capsid-Like External Scaffold of Immature Virions during Vaccinia Virus Morphogenesis. J. Virol.
83: 9140-9150
[Abstract] [Full Text] -
Jalasvuori, M., Jaatinen, S. T., Laurinavicius, S., Ahola-Iivarinen, E., Kalkkinen, N., Bamford, D. H., Bamford, J. K. H.
(2009). The Closest Relatives of Icosahedral Viruses of Thermophilic Bacteria Are among Viruses and Plasmids of the Halophilic Archaea. J. Virol.
83: 9388-9397
[Abstract] [Full Text] -
Wu, G. A., Jun, S.-R., Sims, G. E., Kim, S.-H.
(2009). Whole-proteome phylogeny of large dsDNA virus families by an alignment-free method. Proc. Natl. Acad. Sci. USA
106: 12826-12831
[Abstract] [Full Text] -
Jeudy, S., Lartigue, A., Claverie, J.-M., Abergel, C.
(2009). Dissecting the Unique Nucleotide Specificity of Mimivirus Nucleoside Diphosphate Kinase. J. Virol.
83: 7142-7150
[Abstract] [Full Text] -
Cherrier, M. V., Kostyuchenko, V. A., Xiao, C., Bowman, V. D., Battisti, A. J., Yan, X., Chipman, P. R., Baker, T. S., Van Etten, J. L., Rossmann, M. G.
(2009). An icosahedral algal virus has a complex unique vertex decorated by a spike. Proc. Natl. Acad. Sci. USA
106: 11085-11089
[Abstract] [Full Text] -
Liao, Y.-C., Shih, Y.-P., Lo, S. H.
(2008). Mutations in the Focal Adhesion Targeting Region of Deleted in Liver Cancer-1 Attenuate Their Expression and Function. Cancer Res.
68: 7718-7722
[Abstract] [Full Text] -
Hyun, J.-K., Coulibaly, F., Turner, A. P., Baker, E. N., Mercer, A. A., Mitra, A. K.
(2007). The Structure of a Putative Scaffolding Protein of Immature Poxvirus Particles as Determined by Electron Microscopy Suggests Similarity with Capsid Proteins of Large Icosahedral DNA Viruses. J. Virol.
81: 11075-11083
[Abstract] [Full Text] -
Ogata, H., Claverie, J.-M.
(2007). Unique genes in giant viruses: Regular substitution pattern and anomalously short size. Genome Res
17: 1353-1361
[Abstract] [Full Text] -
Wang, Y., Kleespies, R. G., Huger, A. M., Jehle, J. A.
(2007). The Genome of Gryllus bimaculatus Nudivirus Indicates an Ancient Diversification of Baculovirus-Related Nonoccluded Nudiviruses of Insects. J. Virol.
81: 5395-5406
[Abstract] [Full Text] -
Bidle, K. D., Haramaty, L., Barcelos e Ramos, J., Falkowski, P.
(2007). Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc. Natl. Acad. Sci. USA
104: 6049-6054
[Abstract] [Full Text] -
Boyle, K. A., Arps, L., Traktman, P.
(2007). Biochemical and Genetic Analysis of the Vaccinia Virus D5 Protein: Multimerization-Dependent ATPase Activity Is Required To Support Viral DNA Replication. J. Virol.
81: 844-859
[Abstract] [Full Text] -
Liao, Y.-C., Si, L., deVere White, R. W., Lo, S. H.
(2007). The phosphotyrosine-independent interaction of DLC-1 and the SH2 domain of cten regulates focal adhesion localization and growth suppression activity of DLC-1. JCB
176: 43-49
[Abstract] [Full Text] -
Renesto, P., Abergel, C., Decloquement, P., Moinier, D., Azza, S., Ogata, H., Fourquet, P., Gorvel, J.-P., Claverie, J.-M.
(2006). Mimivirus Giant Particles Incorporate a Large Fraction of Anonymous and Unique Gene Products. J. Virol.
80: 11678-11685
[Abstract] [Full Text] -
Epifano, C., Krijnse-Locker, J., Salas, M. L., Salas, J., Rodriguez, J. M.
(2006). Generation of Filamentous Instead of Icosahedral Particles by Repression of African Swine Fever Virus Structural Protein pB438L. J. Virol.
80: 11456-11466
[Abstract] [Full Text] -
Osheroff, N.
(2006). Unraveling the Structure of the Variola Topoisomerase IB-DNA Complex: A Possible New Twist on Smallpox Therapy.. Mol. Interv.
6: 245-248
[Abstract] [Full Text] -
Allen, M. J., Forster, T., Schroeder, D. C., Hall, M., Roy, D., Ghazal, P., Wilson, W. H.
(2006). Locus-specific gene expression pattern suggests a unique propagation strategy for a giant algal virus.. J. Virol.
80: 7699-7705
[Abstract] [Full Text] -
Su, H.-P., Lin, D. Y.-w., Garboczi, D. N.
(2006). The structure of g4, the poxvirus disulfide oxidoreductase essential for virus maturation and infectivity.. J. Virol.
80: 7706-7713
[Abstract] [Full Text] -
Ilouze, M., Dishon, A., Kotler, M.
(2006). Characterization of a Novel Virus Causing a Lethal Disease in Carp and Koi. Microbiol. Mol. Biol. Rev.
70: 147-156
[Abstract] [Full Text] -
Allen, M. J., Schroeder, D. C., Holden, M. T. G., Wilson, W. H.
(2006). Evolutionary History of the Coccolithoviridae. Mol Biol Evol
23: 86-92
[Abstract] [Full Text] -
Suhre, K.
(2005). Gene and Genome Duplication in Acanthamoeba polyphaga Mimivirus. J. Virol.
79: 14095-14101
[Abstract] [Full Text] -
Suhre, K., Audic, S., Claverie, J.-M.
(2005). Mimivirus gene promoters exhibit an unprecedented conservation among all eukaryotes. Proc. Natl. Acad. Sci. USA
102: 14689-14693
[Abstract] [Full Text] -
Bubeck, J. A., Pfitzner, A. J. P.
(2005). Isolation and characterization of a new type of chlorovirus that infects an endosymbiotic Chlorella strain of the heliozoon Acanthocystis turfacea. J. Gen. Virol.
86: 2871-2877
[Abstract] [Full Text] -
Szajner, P., Weisberg, A. S., Lebowitz, J., Heuser, J., Moss, B.
(2005). External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. JCB
170: 971-981
[Abstract] [Full Text] -
Wilson, W. H., Schroeder, D. C., Allen, M. J., Holden, M. T. G., Parkhill, J., Barrell, B. G., Churcher, C., Hamlin, N., Mungall, K., Norbertczak, H., Quail, M. A., Price, C., Rabbinowitsch, E., Walker, D., Craigon, M., Roy, D., Ghazal, P.
(2005). Complete Genome Sequence and Lytic Phase Transcription Profile of a Coccolithovirus. Science
309: 1090-1092
[Abstract] [Full Text] -
Bamford, D. H., Ravantti, J. J., Ronnholm, G., Laurinavicius, S., Kukkaro, P., Dyall-Smith, M., Somerharju, P., Kalkkinen, N., Bamford, J. K. H.
(2005). Constituents of SH1, a Novel Lipid-Containing Virus Infecting the Halophilic Euryarchaeon Haloarcula hispanica. J. Virol.
79: 9097-9107
[Abstract] [Full Text] -
Yan, X., Chipman, P. R., Castberg, T., Bratbak, G., Baker, T. S.
(2005). The Marine Algal Virus PpV01 Has an Icosahedral Capsid with T=219 Quasisymmetry. J. Virol.
79: 9236-9243
[Abstract] [Full Text] -
Iyer, L. M., Koonin, E. V., Leipe, D. D., Aravind, L.
(2005). Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucleic Acids Res
33: 3875-3896
[Abstract] [Full Text] -
Ogata, H., Abergel, C., Raoult, D., Claverie, J.-M.
(2005). Response to Comment on "The 1.2-Megabase Genome Sequence of Mimivirus". Science
308: 1114b-1114b
[Full Text] -
Heuser, J.
(2005). Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic "honeycomb" surface coat. JCB
169: 269-283
[Abstract] [Full Text] -
Lucet, I. S., Tynan, F. E., Adams, V., Rossjohn, J., Lyras, D., Rood, J. I.
(2005). Identification of the Structural and Functional Domains of the Large Serine Recombinase TnpX from Clostridium perfringens. J. Biol. Chem.
280: 2503-2511
[Abstract] [Full Text] -
Raoult, D., Audic, S., Robert, C., Abergel, C., Renesto, P., Ogata, H., La Scola, B., Suzan, M., Claverie, J.-M.
(2004). The 1.2-Megabase Genome Sequence of Mimivirus. Science
306: 1344-1350
[Abstract] [Full Text] -
Espagne, E., Dupuy, C., Huguet, E., Cattolico, L., Provost, B., Martins, N., Poirie, M., Periquet, G., Drezen, J. M.
(2004). Genome Sequence of a Polydnavirus: Insights into Symbiotic Virus Evolution. Science
306: 286-289
[Abstract] [Full Text] -
Iyer, L. M., Makarova, K. S., Koonin, E. V., Aravind, L.
(2004). Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. Nucleic Acids Res
32: 5260-5279
[Abstract] [Full Text] -
Markine-Goriaynoff, N., Gillet, L., Van Etten, J. L., Korres, H., Verma, N., Vanderplasschen, A.
(2004). Glycosyltransferases encoded by viruses. J. Gen. Virol.
85: 2741-2754
[Abstract] [Full Text] -
Greub, G., Raoult, D.
(2004). Microorganisms Resistant to Free-Living Amoebae. Clin. Microbiol. Rev.
17: 413-433
[Abstract] [Full Text] -
Stasiak, K., Renault, S., Demattei, M.-V., Bigot, Y., Federici, B. A.
(2003). Evidence for the evolution of ascoviruses from iridoviruses. J. Gen. Virol.
84: 2999-3009
[Abstract] [Full Text] -
Bideshi, D. K., Renault, S., Stasiak, K., Federici, B. A., Bigot, Y.
(2003). Phylogenetic analysis and possible function of bro-like genes, a multigene family widespread among large double-stranded DNA viruses of invertebrates and bacteria. J. Gen. Virol.
84: 2531-2544
[Abstract] [Full Text] -
Hughes, A. L., Friedman, R.
(2003). Genome-Wide Survey for Genes Horizontally Transferred from Cellular Organisms to Baculoviruses. Mol Biol Evol
20: 979-987
[Abstract] [Full Text] -
Scola, B. L., Audic, S., Robert, C., Jungang, L., de Lamballerie, X., Drancourt, M., Birtles, R., Claverie, J.-M., Raoult, D.
(2003). A Giant Virus in Amoebae. Science
299: 2033-2033
[Full Text] -
Heath, C. M., Windsor, M., Wileman, T.
(2003). Membrane Association Facilitates the Correct Processing of pp220 during Production of the Major Matrix Proteins of African Swine Fever Virus. J. Virol.
77: 1682-1690
[Abstract] [Full Text] -
Gong, C., Shuman, S.
(2002). Chlorella Virus RNA Triphosphatase. MUTATIONAL ANALYSIS AND MECHANISM OF INHIBITION BY TRIPOLYPHOSPHATE. J. Biol. Chem.
277: 15317-15324
[Abstract] [Full Text]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Copyright © 2009 by the American Society for Microbiology. For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»