Eukaryotic Circular Rep-Encoding Single-Stranded DNA (CRESS DNA) Viruses: Ubiquitous Viruses With Small Genomes and a Diverse Host Range

doi:10.1016/bs.aivir.2018.10.001

Advances in Virus Research

Volume 103, 2019, Pages 71-133

https://doi.org/10.1016/bs.aivir.2018.10.001 Get rights and content

Abstract

While single-stranded DNA (ssDNA) was once thought to be a relatively rare genomic architecture for viruses, modern metagenomics sequencing has revealed circular ssDNA viruses in most environments and in association with diverse hosts. In particular, circular ssDNA viruses encoding a homologous replication-associated protein (Rep) have been identified in the majority of eukaryotic supergroups, generating interest in the ecological effects and evolutionary history of circular Rep-encoding ssDNA viruses (CRESS DNA) viruses. This review surveys the explosion of sequence diversity and expansion of eukaryotic CRESS DNA taxonomic groups over the last decade, highlights similarities between the well-studied geminiviruses and circoviruses with newly identified groups known only through their genome sequences, discusses the ecology and evolution of eukaryotic CRESS DNA viruses, and speculates on future research horizons.

Section snippets

Defining CRESS DNA Viruses

The term CRESS DNA viruses was coined in 2012 to refer to a group of single-stranded DNA (ssDNA) viruses encoding a replication-associated protein (Rep) that appears to be descended from a common ancestor. CRESS DNA stands for circular, Rep-encoding ssDNA and encompasses both prokaryotic and eukaryotic viruses, although the Reps of each of these groups have distinct characteristics (Koonin and Ilyina, 1993). Most ssDNA viruses are CRESS DNA viruses. Eleven out of thirteen ssDNA virus families

Discovery of Eukaryotic CRESS DNA Viruses

Although the first eukaryotic CRESS DNA viruses were only identified as such in the 1970s, symptoms consistent with CRESS DNA viral infection were described over a millennium ago. The common yellowing symptom of CRESS DNA viral infection of euphorbia leaves was the inspiration for a Japanese poet in 752 AD (Saunders et al., 2003), though the symptoms are not distinct enough for a definitive retrospective diagnosis. More definitively, plants with symptoms caused by geminiviruses were first

Unity and Diversity

While some eukaryotic CRESS DNA viruses have up to 10 open reading frames (ORFs), even the most compact genomes have two ORFs: one encoding the Rep and one encoding a capsid protein (CP). The conserved Rep serves as the anchor for this group of viruses, but the CP is highly divergent. Beyond the Rep and CP, protein content differs dramatically among CRESS DNA viruses.

Distribution and Sampling

We are not sure how close to the tip of the iceberg virologists are in terms of uncovering CRESS DNA viral diversity, but recent global efforts have more than doubled the number of eukaryotic CRESS DNA viral species in GenBank over the last 10 years (let alone the new strain sequences that add to our appreciation of the diversity within some eukaryotic CRESS DNA viral species). These abundant sequences come from a huge range of hosts and environments, and include both opportunistic sampling and

Eukaryotic CRESS DNA Viruses Evolve Quickly

Evolutionary study of eukaryotic CRESS DNA viruses is not restricted to paleovirology and untangling the deep phylogenetic relationships among families. Some eukaryotic CRESS DNA viruses are emergent pathogens, and the year-to-year evolution of these viruses impacts food security. For instance, novel begomoviruses have been a persistent emerging problem in crops including tomato (Ribeiro et al., 2003). Like emergent RNA viruses, eukaryotic CRESS DNA viruses have been shown to evolve quickly, a

Conclusions

Eukaryotic CRESS DNA viruses have been on the vanguard of the transition from detailed, molecular characterization of novel viruses to taxonomy by sequence similarity alone. Their small genome size, prevalence and affinity for rolling-circle replication allow easy molecular surveillance and high return on sampling effort. Virologists can now appreciate their incredible sequence diversity: varied genomic organization, divergence of the homologous Rep protein and novel viral proteins, which are

Acknowledgments

All authors acknowledge funding from the NSF Assembling the Tree of Life program (DEB-1239976 and DEB-1240049) and S.D. acknowledges funding from NSF OIA 1545553.

The nomenclature for this group of viruses has evolved over the last decade, and the authors would like to acknowledge the input of several ICTV members at the 2018 American Society for Virology meeting for the suggestions, including Poliane Alfenas-Zerbini, Mart Krupovic, Arvind Varsani and Murilo Zerbini.

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Chapter Three - Eukaryotic Circular Rep-Encoding Single-Stranded DNA (CRESS DNA) Viruses: Ubiquitous Viruses With Small Genomes and a Diverse Host Range

Abstract

Section snippets

Defining CRESS DNA Viruses

Discovery of Eukaryotic CRESS DNA Viruses

Unity and Diversity

Distribution and Sampling

Eukaryotic CRESS DNA Viruses Evolve Quickly

Conclusions

Acknowledgments

Virology

Prev. Vet. Med.

Vet. Microbiol.

Virus Res.

Trends Ecol. Evol.

Virology

Virus Res.

Virology

J. Biol. Chem.

Virology

Virus Res.

J. Comp. Pathol.

Adv. Virus Res.

Virology

Infect. Genet. Evol.

Virus Res.

Infect. Genet. Evol.

Infect. Genet. Evol.

Infect. Genet. Evol.

Infect. Genet. Evol.

Virology

Virology

Curr. Opin. Struct. Biol.

Two distinct nanovirus species infecting faba bean in Morocco

Arch. Virol.

Three distinct nanoviruses, one of which represents a new species, infect Faba bean in Ethiopia

Plant Dis.

Time-dependent rate phenomenon in viruses

J. Virol.

Description of a novel monopartite Geminivirus and its defective subviral genome in grapevine

Phytopathology

Cassava mosaic disease: a curse to food security in sub-Saharan Africa

APSnet Features

Spread of bunchy top disease in established banana plantations

Aust. J. Agr. Res.

The marine viromes of four oceanic regions

PLoS Biol.

High-frequency reversion of Geminivirus replication protein mutants during infection

J. Virol.

Notes on Psephotus haematonotus, the red-rumped grass Parrakeet

Avicultural Magazine

Analysis of multiple copies of geminiviral DNA in the genome of four closely related Nicotiana species suggest a unique integration event

Plant Mol. Biol.

First detection of Faba bean necrotic yellow virus in Spain

Plant Dis.

Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution

Proc. Natl. Acad. Sci. U.S.A.

Sequences from ancestral single-stranded DNA viruses in vertebrate genomes: the Parvoviridae and Circoviridae are more than 40 to 50 million years old

J. Virol.

Distribution and inferred evolutionary characteristics of a chimeric ssDNA virus associated with intertidal marine isopods

Viruses

Distribution of circular single-stranded DNA viruses associated with benthic amphipods of genus Diporeia in the Laurentian Great Lakes

Freshw. Biol.

Gene expression of benthic amphipods (genus: Diporeia) in relation to a circular ssDNA virus across two Laurentian Great Lakes

PeerJ

Localizing viruses in their insect vectors

Annu. Rev. Phytopathol.

Novel circular DNA viruses in stool samples of wild-living chimpanzees

J. Gen. Virol.

Molecular detection and genome analysis of circoviruses of European eel (Anguilla anguilla) and Sichel (Pelecus cultratus)

Acta Vet. Hung.

Method for discovering novel DNA viruses in blood using viral particle selection and shotgun sequencing

Biotechniques

Discovery, prevalence, and persistence of novel circular single-stranded DNA viruses in the ctenophores Mnemiopsis leidyi and Beroe ovata

Front. Microbiol.

ICTV virus taxonomy profile: circoviridae

J. Gen. Virol.

Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites

Arch. Virol.

Revision of Begomovirus taxonomy based on pairwise sequence comparisons