Abstract
The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding single-stranded DNA (ssDNA) (CRESS-DNA) viruses that encode capsid proteins that are most closely related to those encoded by RNA viruses in the family Tombusviridae The apparent chimeric nature of the two core proteins encoded by crucivirus genomes suggests horizontal gene transfer of capsid genes between DNA and RNA viruses. Here, we identified and characterized 451 new crucivirus genomes and 10 capsid-encoding circular genetic elements through de novo assembly and mining of metagenomic data. These genomes are highly diverse, as demonstrated by sequence comparisons and phylogenetic analysis of subsets of the protein sequences they encode. Most of the variation is reflected in the replication-associated protein (Rep) sequences, and much of the sequence diversity appears to be due to recombination. Our results suggest that recombination tends to occur more frequently among groups of cruciviruses with relatively similar capsid proteins and that the exchange of Rep protein domains between cruciviruses is rarer than intergenic recombination. Additionally, we suggest members of the stramenopiles/alveolates/Rhizaria supergroup as possible crucivirus hosts. Altogether, we provide a comprehensive and descriptive characterization of cruciviruses.IMPORTANCE Viruses are the most abundant biological entities on Earth. In addition to their impact on animal and plant health, viruses have important roles in ecosystem dynamics as well as in the evolution of the biosphere. Circular Rep-encoding single-stranded (CRESS) DNA viruses are ubiquitous in nature, many are agriculturally important, and they appear to have multiple origins from prokaryotic plasmids. A subset of CRESS-DNA viruses, the cruciviruses, have homologues of capsid proteins encoded by RNA viruses. The genetic structure of cruciviruses attests to the transfer of capsid genes between disparate groups of viruses. However, the evolutionary history of cruciviruses is still unclear. By collecting and analyzing cruciviral sequence data, we provide a deeper insight into the evolutionary intricacies of cruciviruses. Our results reveal an unexpected diversity of this virus group, with frequent recombination as an important determinant of variability.
Highlights
IMPORTANCE Viruses are the most abundant biological entities on Earth
To broaden our understanding of the diversity and relationships of cruciviruses, 461 uncharacterized circular DNA sequences containing predicted coding sequences (CDSs) with sequence similarity to the capsid protein of tombusviruses were compiled from metagenomic sequencing data
The average GC content of the newly described cruciviral sequences is 42.9% Ϯ 4.9% (Fig. 1B) with genome lengths spanning from 2,474 to 7,947 bases (Fig. 1A), some exceeding the size of described bacilladnaviruses (Յ6,000 nucleotides [nt] [53]), the largest Circular Rep-encoding single-stranded (CRESS)-DNA viruses known [12]
Summary
IMPORTANCE Viruses are the most abundant biological entities on Earth. In addition to their impact on animal and plant health, viruses have important roles in ecosystem dynamics as well as in the evolution of the biosphere. Virus variability is driven by various mutation rates, recombination, and reassortment of genetic components [6] These attributes, coupled with many types of genomes (RNA or DNA, single or double stranded, and circular or linear), lead to a large genetic diversity in the “viral world.”. Viral genetic information is coded in either RNA or DNA These genomes can be single (positive or negative sense) or double stranded, or linear or circular, and can be comprised of a single or multiple molecules of nucleic acid (monopartite or multipartite, respectively). The highly abundant circular Rep-encoding single-stranded DNA (CRESS-DNA; Rep being the replication-associated protein) viruses may have been derived from plasmids on multiple occasions by acquiring capsid genes from RNA viruses [9,10,11]. Many CRESS-DNA viruses have been identified in apparently healthy organisms, and metagenomic studies have revealed their presence in most environments [13]
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