Previously unknown and highly divergent ssDNA viruses populate the oceans

Abstract

Single-stranded DNA (ssDNA) viruses are economically important pathogens of plants and animals, and are widespread in oceans; yet, the diversity and evolutionary relationships among marine ssDNA viruses remain largely unknown. Here we present the results from a metagenomic study of composite samples from temperate (Saanich Inlet, 11 samples; Strait of Georgia, 85 samples) and subtropical (46 samples, Gulf of Mexico) seawater. Most sequences (84%) had no evident similarity to sequenced viruses. In total, 608 putative complete genomes of ssDNA viruses were assembled, almost doubling the number of ssDNA viral genomes in databases. These comprised 129 genetically distinct groups, each represented by at least one complete genome that had no recognizable similarity to each other or to other virus sequences. Given that the seven recognized families of ssDNA viruses have considerable sequence homology within them, this suggests that many of these genetic groups may represent new viral families. Moreover, nearly 70% of the sequences were similar to one of these genomes, indicating that most of the sequences could be assigned to a genetically distinct group. Most sequences fell within 11 well-defined gene groups, each sharing a common gene. Some of these encoded putative replication and coat proteins that had similarity to sequences from viruses infecting eukaryotes, suggesting that these were likely from viruses infecting eukaryotic phytoplankton and zooplankton.

Virus taxonomy in the age of metagenomics

“…A recent comprehensive metagenomic analysis of thousands of diverse samples has led to the discovery of approximately 125,000 new viral genomes and a 16-fold increase in the number of identified viral genes 24 . Similarly, as technology advances, it is becoming clear that ssDNA and RNA viruses in marine and other ecosystems are far more diverse than currently characterized viruses; however, these new viruses remain understudied despite their ecological importance 11,[25][26][27][28][29][30][31] . Many ssDNA viruses identified in metagenomic data encode an evolutionarily conserved replication-associated protein (Rep), whereas the number, orientation and evolutionary origin of other genes are highly variable in these circular Rep-encoding ssDNA viruses (CRESS-DNA viruses) 32 .…”

“…However, these sequenced viruses lack information about their hosts and other biological properties that would guide their assignment into species and genera in the family 10 . Indeed, vast numbers of complete, or nearly complete, genome sequences have been assembled and characterized from metagenomic data for viruses with small [11][12][13][14] , medium [15][16][17][18] and even large 19,20 genomes. The identification of entirely new groups of viruses from such analyses emphasizes the power of metagenomic approaches in discovering viruses, some of which could have key functions in the regulation of ecosystems, whereas others could coexist with their hosts without causing recognizable disease or may even be mutualists 7 .…”

A New Microviridae Phage Isolated from a Failed Biotechnological Process Driven by Escherichia coli

“…Phage phiX174 was the very first whole genome to be sequenced and the first virus for which the complete structure was determined. While phages similar to phiX174 have been reported to be abundant in the environment, they are challenging to isolate (25). We believe that isolation and characterization of additional Microviridae phages are key to a better understanding of the evolution of members of this phage family in their natural environment.…”

“…The first approach involves replication of viruses in a chemostat with and without different selective pressures for many generations (15)(16)(17)(18)(19)(20)(21)(22)(23). The second approach is based on isolating and sequencing novel members of the virus family (24) and surveying environmental sequences (25). A recent review on evolutionary studies showed that Microviridae phages undergo parallel evolution, meaning that a common ancestor evolved the same molecular substitutions even when different selective pressures were used (26).…”

Novel ssDNA Viruses Detected in the Virome of Bleached, Habitat-Forming Kelp Ecklonia radiata

“…ssDNA viruses include a subgroup which possess circular genomes, and a particular replication initiation gene, rep. These are therefore called Circular Rep-Encoding ssDNA (CRESS-DNA) viruses (Rosario et al, 2009;Delwart and Li, 2012;Labonté and Suttle, 2013;Simmonds et al, 2017). These include the Geminiviridae, Nanoviridae, Circoviridae, and Genomoviridae, which employ rolling-circle replication (RCR), facilitated by the Rep protein (Rosario et al, 2012b).…”