Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes

Abstract

The genomes of numerous circoviruses and distantly related circular ssDNA viruses encoding a rolling circle replication initiator protein (Rep) have been characterized from the tissues of mammals, fish, insects, plants (geminivirus and nanovirus), in human and animal feces, in an algae cell, and in diverse environmental samples. We review the genome organization, phylogenetic relationships and initial prevalence studies of cycloviruses, a proposed new genus in the Circoviridae family. Viral fossil rep sequences were also recently identified integrated on the chromosomes of mammals, frogs, lancelets, crustaceans, mites, gastropods, roundworms, placozoans, hydrozoans, protozoans, land plants, fungi, algae, and phytoplasma bacterias and their plasmids, reflecting the very wide past host range of rep bearing viruses. An ancient origin for viruses with Rep-encoding small circular ssDNA genomes, predating the diversification of eukaryotes, is discussed. The cellular hosts and pathogenicity of many recently described rep-containing circular ssDNA genomes remain to be determined. Future studies of the virome of single cell and multi-cellular eukaryotes are likely to further extend the known diversity and host-range of small rep-containing circular ssDNA viral genomes.

Figure 1

Phylogenetic analysis of circovirus and cyclovirus species based on the complete amino acid sequence of the Rep protein using the neighbour-joining method with p-distance and 1000 bootstrap replicates. The bar represents 10% estimated genetic divergence. The GenBank accession numbers of the Rep sequences of viruses used in the phylogenetic analyses are in Table 1. The Geminivirus pepper golden mosaic virus (U57457) was used as the outgroup.

Figure 2

(A) Genome organization of a subset of representative Rep-encoding genomes from rodent feces. (B) Phylogenetic analysis using Bayesian inference (MrBayes) as described (Ng et al, 2011) of the complete Rep from circovirus-like genomes identified in feces from mammals (red), plants (green), environmental samples and an algae (blue), and unicellular eukaryotes (yellow). Numbers above each node represent posterior probabilities of the Bayesian analysis. Branch lengths are based on the number of inferred amino acid substitutions, as indicated by the bar (0.3 substitutions per amino acid position).