The high mutation rate of RNA viruses is credited with their evolvability and virulence. This Primer, however, discusses recent evidence that this is, in part, a byproduct of selection for faster ...genomic replication.
Despite their small size and limited protein-coding capacity, the rapid evolution rates of single-stranded DNA (ssDNA) viruses have led to their emergence as serious plant and animal pathogens. ...Recently, metagenomics has revealed an unprecedented diversity of ssDNA viruses, expanding their known environmental distributions and host ranges. This review summarizes and contrasts the basic characteristics of known circular ssDNA viral groups, providing a resource for analyzing the wealth of ssDNA viral sequences identified through metagenomics. Since ssDNA viruses are largely identified based on conserved rolling circle replication proteins, this review highlights distinguishing motifs and catalytic residues important for replication. Genomes identified through metagenomics have demonstrated unique ssDNA viral genome architectures and revealed characteristics that blur the boundaries between previously well-defined groups. Metagenomic discovery of ssDNA viruses has created both a challenge to current taxonomic classification schemes and an opportunity to revisit hypotheses regarding the evolutionary history of these viruses.
Understanding the factors that determine the rate at which genomes generate and fix mutations provides important insights into key evolutionary mechanisms. We review our current knowledge of the ...rates of mutation and substitution, as well as their determinants, in RNA viruses, DNA viruses and retroviruses. We show that the high rate of nucleotide substitution in RNA viruses is matched by some DNA viruses, suggesting that evolutionary rates in viruses are explained by diverse aspects of viral biology, such as genomic architecture and replication speed, and not simply by polymerase fidelity.
Single-stranded DNA (ssDNA) viruses with circular genomes are the smallest viruses known to infect eukaryotes. The present study identified 10 novel genomes similar to ssDNA circoviruses through ...data-mining of public viral metagenomes. The metagenomic libraries included samples from reclaimed water and three different marine environments (Chesapeake Bay, British Columbia coastal waters and Sargasso Sea). All the genomes have similarities to the replication (Rep) protein of circoviruses; however, only half have genomic features consistent with known circoviruses. Some of the genomes exhibit a mixture of genomic features associated with different families of ssDNA viruses (i.e. circoviruses, geminiviruses and parvoviruses). Unique genome architectures and phylogenetic analysis of the Rep protein suggest that these viruses belong to novel genera and/or families. Investigating the complex community of ssDNA viruses in the environment can lead to the discovery of divergent species and help elucidate evolutionary links between ssDNA viruses.
Whole-genome shotgun sequence data from three individual cells isolated from seawater, followed by analysis of ribosomal DNA, indicated that the cells represented three divergent clades of ...picobiliphytes. In contrast with the recent description of this phylum, we found no evidence of plastid DNA nor of nuclear-encoded plastid-targeted proteins, which suggests that these picobiliphytes are heterotrophs. Genome data from one cell were dominated by sequences from a widespread single-stranded DNA virus. This virus was absent from the other two cells, both of which contained non-eukaryote DNA derived from marine Bacteroidetes and large DNA viruses. By using shotgun sequencing of uncultured marine picobiliphytes, we revealed the distinct interactions of individual cells.
The rapidly expanding phylum
Cressdnaviricota
contains circular, Rep-encoding single-stranded (CRESS) DNA viruses that are organized within seven established families, but many CRESS DNA virus ...sequences are not taxonomically defined. We hypothesized that genes in CRESS DNA virus ambisense genomes exhibit strand-specific signatures due to a cytosine to thymine transition bias that can help determine the orientation of the genome: which strand is packaged and is in the “virion sense”. To identify broad strand-specific patterns across genera, we performed compositional analyses of codon usage across the two major opposite sense open reading frames of 712 reference viruses. Additionally, we developed a statistical test to identify relative codon overrepresentation between ambisense sequence pairs for each classified virus exemplar and an additional 137 unclassified CRESS DNA viruses. Codons clustered by the identity of their third-position nucleotide, displaying both strand- and genus-specific patterns across
Cressdnaviricota
. Roughly 70% of virion-sense sequences have a relative overrepresentation of thymine-ending codons while ~80% of anti-sense sequences display a relative overrepresentation of adenine-ending codons (corresponding to a relative overrepresentation of thymine in these genes as packaged). Thirteen of the 137 unclassified viruses show strong evidence of having the rarer circovirus-like genome orientation, and likely represent novel genera or families within
Cressdnaviricota
. Given the strong strand-specific patterns of relative codon overrepresentation, the results suggest that the relative codon overrepresentation test can serve as a tool to help corroborate the genome organization of unclassified CRESS DNA viruses.
The high rates of RNA virus evolution are generally attributed to replication with error-prone RNA-dependent RNA polymerases. However, these long-term nucleotide substitution rates span three orders ...of magnitude and do not correlate well with mutation rates or selection pressures. This substitution rate variation may be explained by differences in virus ecology or intrinsic genomic properties. We generated nucleotide substitution rate estimates for mammalian RNA viruses and compiled comparable published rates, yielding a dataset of 118 substitution rates of structural genes from 51 different species, as well as 40 rates of non-structural genes from 28 species. Through ANCOVA analyses, we evaluated the relationships between these rates and four ecological factors: target cell, transmission route, host range, infection duration; and three genomic properties: genome length, genome sense, genome segmentation. Of these seven factors, we found target cells to be the only significant predictors of viral substitution rates, with tropisms for epithelial cells or neurons (P<0.0001) as the most significant predictors. Further, one-tailed t-tests showed that viruses primarily infecting epithelial cells evolve significantly faster than neurotropic viruses (P<0.0001 and P<0.001 for the structural genes and non-structural genes, respectively). These results provide strong evidence that the fastest evolving mammalian RNA viruses infect cells with the highest turnover rates: the highly proliferative epithelial cells. Estimated viral generation times suggest that epithelial-infecting viruses replicate more quickly than viruses with different cell tropisms. Our results indicate that cell tropism is a key factor in viral evolvability.
Current knowledge of plant virus diversity is biased towards agents of visible and economically important diseases. Less is known about viruses that have not caused major diseases in crops, or ...viruses from native vegetation, which are a reservoir of biodiversity that can contribute to viral emergence. Discovery of these plant viruses is hindered by the traditional approach of sampling individual symptomatic plants. Since many damaging plant viruses are transmitted by insect vectors, we have developed "vector-enabled metagenomics" (VEM) to investigate the diversity of plant viruses. VEM involves sampling of insect vectors (in this case, whiteflies) from plants, followed by purification of viral particles and metagenomic sequencing. The VEM approach exploits the natural ability of highly mobile adult whiteflies to integrate viruses from many plants over time and space, and leverages the capability of metagenomics for discovering novel viruses. This study utilized VEM to describe the DNA viral community from whiteflies (Bemisia tabaci) collected from two important agricultural regions in Florida, USA. VEM successfully characterized the active and abundant viruses that produce disease symptoms in crops, as well as the less abundant viruses infecting adjacent native vegetation. PCR assays designed from the metagenomic sequences enabled the complete sequencing of four novel begomovirus genome components, as well as the first discovery of plant virus satellites in North America. One of the novel begomoviruses was subsequently identified in symptomatic Chenopodium ambrosiodes from the same field site, validating VEM as an effective method for proactive monitoring of plant viruses without a priori knowledge of the pathogens. This study demonstrates the power of VEM for describing the circulating viral community in a given region, which will enhance our understanding of plant viral diversity, and facilitate emerging plant virus surveillance and management of viral diseases.
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