Diverse circovirus-like genome architectures revealed by environmental metagenomics

Abstract

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.

Previously unknown and highly divergent ssDNA viruses populate the oceans

“…About 1.6% of the total sequences were homologous to the genus Gokushovirus from the Microviridae. Previous studies found that viruses in the Circoviridae and Microviridae (Gokushovirus) are widespread in marine and fresh waters (Angly et al, 2006;Rosario et al, 2009). As well, some aquatic circovirus-like sequences appear to encode a capsid protein known previously only in RNA viruses (Diemer and Stedman, 2012).…”

“…Feature frequency profiles and network representation BLAST was used to compare the complete circular genomes with those from the NCBI database, including sequenced isolates infecting plants, animals and bacteria, as well as environmental genomes from other metagenomic libraries (10 circovirus-like genomes from an Antarctic lake (Ló pez-Bueno et al, 2009), 9 from marine environments (Rosario et al, 2009) and 11 cycloviruses from chimpanzee stools (Li et al, 2010)). Only the NCBI genomes that were similar to at least one environmental genome were kept for further analysis.…”

“…Sequences with similarity to ssDNA viruses have been found in metagenomic data from multiple environments (reviewed in Rosario and Breitbart, 2011;Rosario et al, 2012). For example, sequences from the Microviridae and Circoviridae have been observed in marine environments (Angly et al, 2006;Rosario et al, 2009), freshwater (Ló pez-Bueno et al, 2009) and modern stromatolites , and similar to those from the Circoviridae, Geminiviridae, Nanoviridae and Parvoviridae were observed in corals (Thurber et al, 2008). However, the identification of ssDNA viruses relies on comparative analysis with sequences in databases that do not adequately reflect the diversity of ssDNA in nature; hence, the diversity of ssDNA viruses remains poorly characterized.…”

Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean

“…However, at this time, the number of marine ssDNA viruses that have been cultured in the laboratory is extremely limited. Metagenomic studies including a multiple displacement amplification step, which is known to enrich for small, circular, ssDNA genomes (Haible et al, 2006;Kim et al, 2008), have identified numerous sequences from ssDNA viruses (including both phages and eukaryotic viruses) in marine environments (Angly et al, 2006;Wegley et al, 2007;Desnues et al, 2008;Rosario et al, 2009). However, the ecology of the ssDNA viruses identified through metagenomic sequencing is completely unknown.…”

Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses

“…Many of these uncultivated viruses are related to members of the bacteriophage family Microviridae 9 , but perhaps even larger number encode RC-Reps displaying phylogenetic affinity to one of three families of eukaryotic ssDNA viruses-Circoviridae, Geminiviridae and Nanoviridae (for example, see refs [24][25][26][27]. Interestingly, instead of encoding genes for corresponding CPs (circo-, gemini-and nano-like), these viruses typically bear open-reading frames that do not share appreciable similarity with sequences in the databases.…”