Discovery of several thousand highly diverse circular DNA viruses.

Published on Feb 4, 2020in eLife7.08
· DOI :10.7554/ELIFE.51971
Michael J. Tisza7
Estimated H-index: 7
(NIH: National Institutes of Health),
Diana V. Pastrana30
Estimated H-index: 30
(NIH: National Institutes of Health)
+ 23 AuthorsChristopher B. Buck52
Estimated H-index: 52
(NIH: National Institutes of Health)
Sources
Abstract
When scientists hunt for new DNA sequences, sometimes they get a lot more than they bargained for. Such is the case in metagenomic surveys, which analyze not just DNA of a particular organism, but all the DNA in an environment at large. A vexing problem with these surveys is the overwhelming number of DNA sequences detected that are so different from any known microbe that they cannot be classified using traditional approaches. However, some of these “known unknowns” are undoubtedly viral sequences, because only a fraction of the enormous diversity of viruses has been characterized. This “viral dark matter” is a major obstacle for those studying viruses. This led Tisza et al. to attempt to classify some of the unknown viral sequences in their metagenomic surveys. The search, which specifically focused on viruses with circular DNA genomes, detected over 2,500 circular viral genomes. Intensive analysis revealed that many of these genomes had similar makeup to previously discovered viruses, but hundreds of them were totally different from any known virus, based on typical methods of comparison. Computational analysis of genes that were conserved among some of these brand-new circular sequences often revealed virus-like features. Experiments on a few of these genes showed that they encoded proteins capable of forming particles reminiscent of characteristic viral shells, implying that these new sequences are indeed viruses. Tisza et al. have added the 2,500 newly characterized viral sequences to the publicly accessible GenBank database, and the sequences are being considered for the more authoritative RefSeq database, which currently contains around 9,000 complete viral genomes. The expanded databases will hopefully now better equip scientists to explore the enormous diversity of viruses and help medics and veterinarians to detect disease-causing viruses in humans and other animals.
📖 Papers frequently viewed together
18k Citations
74.5k Citations
125 Citations
References98
Newest
#1Moreno Zolfo (University of Trento)H-Index: 17
#2Federica Pinto (University of Trento)H-Index: 7
Last. Nicola Segata (University of Trento)H-Index: 61
view all 7 authors...
28 CitationsSource
#1Maria Asplund (Wild Center)H-Index: 7
#2Kristín Rós Kjartansdóttir (Wild Center)H-Index: 5
Last. Anders J. Hansen (Wild Center)H-Index: 34
view all 23 authors...
Abstract Objectives Sample preparation for high-throughput sequencing (HTS) includes treatment with various laboratory components, potentially carrying viral nucleic acids, the extent of which has not been thoroughly investigated. Our aim was to systematically examine a diverse repertoire of laboratory components used to prepare samples for HTS in order to identify contaminating viral sequences. Methods A total of 322 samples of mainly human origin were analysed using eight protocols, applying a...
53 CitationsSource
#1Rafaela S. Fontenele (ASU: Arizona State University)H-Index: 10
#2Cristiano Lacorte (Empresa Brasileira de Pesquisa Agropecuária)H-Index: 10
Last. Simone G. Ribeiro (Empresa Brasileira de Pesquisa Agropecuária)H-Index: 18
view all 6 authors...
Capybaras (Hydrochoerus hydrochaeris), the world’s largest rodents, are distributed throughout South America. These wild herbivores are commonly found near water bodies and are well adapted to rural and urban areas. There is limited information on the viruses circulating through capybaras. This study aimed to expand the knowledge on the viral diversity associated with capybaras by sampling their faeces. Using a viral metagenomics approach, we identified diverse single-stranded DNA viruses in the...
16 CitationsSource
#1Darius Kazlauskas (Vilnius University)H-Index: 12
#2Arvind Varsani (ASU: Arizona State University)H-Index: 63
Last. Mart Krupovic (Pasteur Institute)H-Index: 59
view all 4 authors...
Single-stranded (ss) DNA viruses are a major component of the earth virome. In particular, the circular, Rep-encoding ssDNA (CRESS-DNA) viruses show high diversity and abundance in various habitats. By combining sequence similarity network and phylogenetic analyses of the replication proteins (Rep) belonging to the HUH endonuclease superfamily, we show that the replication machinery of the CRESS-DNA viruses evolved, on three independent occasions, from the Reps of bacterial rolling circle-replic...
45 CitationsSource
#1Simon Roux (JGI: Joint Genome Institute)H-Index: 41
#2Mart Krupovic (Pasteur Institute)H-Index: 59
Last. Emiley A. Eloe-Fadrosh (JGI: Joint Genome Institute)H-Index: 28
view all 16 authors...
Bacteriophages from the Inoviridae family (inoviruses) are characterized by their unique morphology, genome content and infection cycle. One of the most striking features of inoviruses is their ability to establish a chronic infection whereby the viral genome resides within the cell in either an exclusively episomal state or integrated into the host chromosome and virions are continuously released without killing the host. To date, a relatively small number of inovirus isolates have been extensi...
89 CitationsSource
#1Pierre LefeuvreH-Index: 29
#2Darren P. Martin (UCT: University of Cape Town)
Last. Arvind Varsani (ASU: Arizona State University)H-Index: 63
view all 6 authors...
The discovery of the first non-cellular infectious agent, later determined to be tobacco mosaic virus, paved the way for the field of virology. In the ensuing decades, research focused on discovering and eliminating viral threats to plant and animal health. However, recent conceptual and methodological revolutions have made it clear that viruses are not merely agents of destruction but essential components of global ecosystems. As plants make up over 80% of the biomass on Earth, plant viruses li...
57 CitationsSource
#1Ivica LetunicH-Index: 53
#2Peer Bork (EMBL-EBI: European Bioinformatics Institute)H-Index: 222
: The Interactive Tree Of Life (https://itol.embl.de) is an online tool for the display, manipulation and annotation of phylogenetic and other trees. It is freely available and open to everyone. The current version introduces four new dataset types, together with numerous new features. Annotation options have been expanded and new control options added for many display elements. An interactive spreadsheet-like editor has been implemented, providing dataset creation and editing directly in the we...
2,380 CitationsSource
#1Simona Kraberger (ASU: Arizona State University)H-Index: 26
#2Kara Schmidlin (ASU: Arizona State University)H-Index: 7
Last. Arvind Varsani (ASU: Arizona State University)H-Index: 63
view all 5 authors...
Over the last decade, arthropods have been shown to harbour a rich diversity of viruses. Through viral metagenomics a large diversity of single-stranded (ss) DNA viruses have been identified. Here we examine the ssDNA virome of the hematophagous New Zealand blackfly using viral metagenomics. Our investigation reveals a plethora of novel ssDNA viral genomes, some of which cluster in the viral families Genomoviridae (n = 9), Circoviridae (n = 1), and Microviridae (n = 108), others in putative fami...
11 CitationsSource
#1Ann C. Gregory (OSU: Ohio State University)H-Index: 14
#2Ahmed A. Zayed (OSU: Ohio State University)H-Index: 9
Last. Simon Roux (OSU: Ohio State University)H-Index: 41
view all 52 authors...
Microbes drive most ecosystems and are modulated by viruses that impact their lifespan, gene flow, and metabolic outputs. However, ecosystem-level impacts of viral community diversity remain difficult to assess due to classification issues and few reference genomes. Here, we establish an ∼12-fold expanded global ocean DNA virome dataset of 195,728 viral populations, now including the Arctic Ocean, and validate that these populations form discrete genotypic clusters. Meta-community analyses revea...
218 CitationsSource
#1Ho Bin Jang (OSU: Ohio State University)H-Index: 18
#2Benjamin Bolduc (OSU: Ohio State University)H-Index: 17
Last. Matthew B. Sullivan (OSU: Ohio State University)H-Index: 75
view all 12 authors...
Microbiomes from every environment contain a myriad of uncultivated archaeal and bacterial viruses, but studying these viruses is hampered by the lack of a universal, scalable taxonomic framework. We present vConTACT v.2.0, a network-based application utilizing whole genome gene-sharing profiles for virus taxonomy that integrates distance-based hierarchical clustering and confidence scores for all taxonomic predictions. We report near-identical (96%) replication of existing genus-level viral tax...
175 CitationsSource
Cited By68
Newest
#1Quinn M. Patterson (ASU: Arizona State University)
#2Simona Kraberger (ASU: Arizona State University)H-Index: 26
Last. Jennifer M. Burns (TTU: Texas Tech University)H-Index: 29
view all 11 authors...
Abstract null null Circoviridae is a family of circular single-stranded DNA viruses whose members infect a wide variety of hosts. While well characterized in avian and mammalian hosts, little is known about circoviruses associated with Antarctic animals. From 48 Weddell seal (Leptonychotes weddellii) fecal samples collected on the sea ice in McMurdo between Nov 2014 and Dec 2014, we identified and determined the genomes of novel viruses that fall within two genera of the family Circoviridae, i.e...
Source
#1Kaihao Tang (CAS: Chinese Academy of Sciences)H-Index: 6
#2Weiquan Wang (CAS: Chinese Academy of Sciences)H-Index: 5
Last. Xiaoxue Wang (CAS: Chinese Academy of Sciences)H-Index: 21
view all 7 authors...
The life cycle of temperate phages includes a lysogenic cycle stage when the phage integrates into the host genome and becomes a prophage. However, the identification of prophages that are highly divergent from known phages remains challenging. In this study, by taking advantage of the lysis-lysogeny switch of temperate phages, we designed Prophage Tracer, a tool for recognizing active prophages in prokaryotic genomes using short-read sequencing data, independent of phage gene similarity searchi...
Source
#1Mart Krupovic (Pasteur Institute)H-Index: 59
#2Arvind Varsani (ASU: Arizona State University)H-Index: 63
The family Smacoviridae (order Cremevirales, class Arfiviricetes, phylum Cressdnaviricota) is comprised of viruses with small circular single-stranded DNA genomes of ~2.3-3 kb in length that have primarily been identified in fecal sample of various animals. Smacovirus genomes carry two genes in ambisense orientation encoding a capsid protein and a rolling-circle replication initiation protein, respectively. We have revised the taxonomy of the family by assigning 138 new genomic sequences deposit...
Source
#1Mona Saleh (University of Veterinary Medicine Vienna)H-Index: 15
#2Boglárka SellyeiH-Index: 7
Last. Csaba SzékelyH-Index: 27
view all 4 authors...
In aquaculture, disease management and pathogen control are key for a successful fish farming industry. In past years, European catfish farming has been flourishing. However, devastating fish pathogens including limiting fish viruses are considered a big threat to further expanding of the industry. Even though mainly the ranavirus (Iridoviridea) and circovirus (Circoviridea) infections are considered well- described in European catfish, more other agents including herpes-, rhabdo or papillomavir...
Source
#1Julian R. Garneau (Pasteur Institute)H-Index: 6
#2Véronique Legrand (Pasteur Institute)
Last. Marc Monot (Pasteur Institute)H-Index: 28
view all 9 authors...
Viruses that infect bacteria (phages) are increasingly recognized for their importance in diverse ecosystems but identifying and annotating them in large-scale sequence datasets is still challenging. Although efficient scalable virus identification tools are emerging, defining the exact ends (termini) of phage genomes is still particularly difficult. The proper identification of termini is crucial, as it helps in characterizing the packaging mechanism of bacteriophages and provides information o...
Source
#3Henry Munyanduki (Vaccine and Infectious Disease Organization)H-Index: 3
The host’s immune status may affect virus evolution. Little is known about how developing fetal and placental immune milieus affect virus heterogeneity. This knowledge will help us better understand intra-host virus evolution and how new virus variants emerge. The goal of our study was to find out whether the isolated in utero environment—an environment with specialized placental immunity and developing fetal immunity—supports the emergence of RNA and DNA virus variants. We used well-established...
Source
#1Ema H. Graham (NU: University of Nebraska–Lincoln)
#2Jennifer Clarke (NU: University of Nebraska–Lincoln)H-Index: 40
Last. Michael S. Adamowicz (NU: University of Nebraska–Lincoln)H-Index: 6
view all 5 authors...
The use of skin virome for human identification purposes offers a unique approach to instances where a viable and statistically relevant human DNA profile is unavailable. The human skin virome may act as an alternative DNA profile and/or an additional form of probative genetic material. To date, no study has attempted to investigate the human virome over a time series across various physical locations of the body to identify its potential as a tool for human identification. For this study, we se...
Source
Last. Souvik GhoshH-Index: 25
view all 4 authors...
Fecal samples from 76 of 83 apparently healthy small Indian mongooses (Urva auropunctata) were PCR positive with circovirus/cyclovirus pan-rep (replicase gene) primers. In this case, 30 samples yielded high quality partial rep sequences (~400 bp), of which 26 sequences shared maximum homology with cycloviruses from an arthropod, bats, humans or a sheep. Three sequences exhibited maximum identities with a bat circovirus, whilst a single sequence could not be assigned to either genus. Using invers...
Source
#1Arvind Varsani (ASU: Arizona State University)H-Index: 63
#2Tanja Opriessnig (Edin.: University of Edinburgh)H-Index: 64
Last. Simona Kraberger (ASU: Arizona State University)H-Index: 26
view all 10 authors...
Anelloviruses are small negative-sense single-stranded DNA viruses with genomes ranging in size from 1.6 to 3.9 kb. The family Anelloviridae comprised 14 genera before the present changes. However, in the last five years, a large number of diverse anelloviruses have been identified in various organisms. Here, we undertake a global analysis of mammalian anelloviruses whose full genome sequences have been determined and have an intact open reading frame 1 (ORF1). We established new criteria for th...
2 CitationsSource
Anelloviruses are a ubiquitous component of healthy human viromes and remain highly prevalent after being acquired early in life. The full extent of "anellome" diversity and its evolutionary dynamics remain unexplored. We employed in-depth sequencing of blood-transfusion donor(s)-recipient pairs coupled with public genomic resources for a large-scale assembly of anellovirus genomes and used the data to characterize global and personal anellovirus diversity through time. The breadth of the anello...
1 CitationsSource