Discovery of several thousand highly diverse circular DNA viruses

Tisza, Michael J.; Pastrana, Diana V.; Welch, Nicole L.; Stewart, Brittany; Peretti, Alberto; Starrett, Gabriel J.; Pang, Yuk Ying S.; Krishnamurthy, Siddharth R.; Pesavento, Patricia A.; McDermott, David H.; Murphy, Philip M.; Whited, Jessica L.; Miller, Bess M.; Brenchley, Jason M.; Rosshart, Stephan P.; Rehermann, Barbara; Doorbar, John; Ta'ala, Blake A; Pletniková, Olga; Troncoso, Juan C.; Resnick, Susan M.; Bolduc, Benjamin; Sullivan, Matthew B.; Varsani, Arvind; Segall, Anca M.; Buck, Christopher B.

doi:10.7554/elife.51971

Cited by 156 publications

(174 citation statements)

References 100 publications

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“…A total of 58 complete circular viral genomes and 3 satellites (circular sequences encoding a Rep similar to those encoded by ssDNA viral genomes but with no discernible capsid protein) were identified and annotated using a combination of the Cenote-taker2 Pipeline and manual screening of the resulting circular contigs (28). The viral genomes ranged in size from a 1.6-kb eukaryotic CRESS DNA virus found in Manatee Springs to a 90-kb prokaryotic dsDNA myovirus recovered from Jackson Springs (see Table S1 in the supplemental material).…”

Section: Resultsmentioning

confidence: 99%

Prokaryotic and Viral Community Composition of Freshwater Springs in Florida, USA

Malki

Rosario

Sawaya

et al. 2020

mBio

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Aquifers, which are essential underground freshwater reservoirs worldwide, are understudied ecosystems that harbor diverse forms of microbial life. This study investigated the abundance and composition of prokaryotic and viral communities in the outflow of five springs across northern Florida, USA, as a proxy of microbial communities found in one of the most productive aquifers in the world, the Floridan aquifer. The average abundances of virus-like particles and prokaryotic cells were slightly lower than those reported from other groundwater systems, ranging from 9.6 × 103 ml−1 to 1.1 × 105 ml−1 and 2.2 × 103 ml−1 to 3.4 × 104 ml−1, respectively. Despite all of the springs being fed by the Floridan aquifer, sequencing of 16S rRNA genes and viral metagenomes (viromes) revealed unique communities in each spring, suggesting that groundwater microbial communities are influenced by land usage in recharge zones. The prokaryotic communities were dominated by Bacteria, and though the most abundant phyla (Proteobacteria, Cyanobacteria, and Bacteroidetes) were found in relatively high abundance across springs, variation was seen at finer taxonomic resolution. The viral sequences were most similar to those described from other aquatic environments. Sequencing resulted in the completion of 58 novel viral genomes representing members of the order Caudovirales as well as prokaryotic and eukaryotic single-stranded DNA (ssDNA) viruses. Sequences similar to those of ssDNA viruses were detected at all spring sites and dominated the identifiable sequences at one spring site, showing that these small viruses merit further investigation in groundwater systems. IMPORTANCE Aquifer systems may hold up to 40% of the total microbial biomass on Earth. However, little is known about the composition of microbial communities within these critical freshwater ecosystems. Here, we took advantage of Florida’s first-magnitude springs (the highest spring classification based on water discharge), each discharging at least 246 million liters of water each day from the Floridan aquifer system (FAS), to investigate prokaryotic and viral communities from the aquifer. The FAS serves as a major source of potable water in the Southeastern United States, providing water for large cities and citizens in three states. Unfortunately, the health of the FAS and its associated springs has declined in the past few decades due to nutrient loading, increased urbanization and agricultural activity in aquifer recharge zones, and saltwater intrusion. This is the first study to describe the prokaryotic and viral communities in Florida’s first-magnitude springs, providing a baseline against which to compare future ecosystem change.

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Section: Resultsmentioning

confidence: 99%

Prokaryotic and Viral Community Composition of Freshwater Springs in Florida, USA

Malki

Rosario

Sawaya

et al. 2020

mBio

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“…Although no other ssDNA phages are known to encode antisense RNA, it is relatively common among ssDNA viruses of eukaryotes. For example, Bean golden yellow mosaic virus, Beet curly top virus, Maize streak virus, Tomato pseudo-curly top virus, Porcine circovirus 1, and Bacilladnavirus all produce antisense RNA that contains genes (Briddon et al, 1996; Gilbertson et al, 1991; Lazarowitz, 1988; Niagro et al, 1998; Stanley et al, 1986; Tisza et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

A high-resolution map of bacteriophage øX174 transcription

Logel

Jaschke

2020

Preprint

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Bacteriophage øX174 is a model virus for studies across the fields of structural biology, genetics, gut microbiome, and synthetic biology, but did not have a high-resolution transcriptome until this work. In this study we used next-generation sequencing to measure the RNA produced from øX174 while infecting its host E. coli C. We broadly confirm the past transcriptome model while revealing several interesting deviations from previous knowledge. Additionally, we measure the strength of canonical øX174 promoters and terminators and discover both a putative new promoter that may be activated by heat shock sigma factors, as well as rediscover a controversial Rho-dependent terminator. We also provide evidence for the first antisense transcription observed in the Microviridae family, identify two promoters that may be involved in generating this transcriptional activity, and discuss possible reasons why this RNA may be produced.

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“…The cruciviral sequences were named sequentially, beginning with the smallest genome, which was named CruV-81 to account for the 80 crucivirus genomes reported in prior literature (15,19,(28)(29)(30)(31)(20)(21)(22)(23)(24)(25)(26)(27). The average GC content of the newly described cruciviral sequences is 42.9 ± 4.9 % ( Fig.…”

Section: Accession Numbersmentioning

confidence: 99%

“…Interestingly, CruV-420 contains not one tombusvirus-related CP, but two. A recent compilation of CRESS-DNA viruses from animal metagenomes also contains four genomes with two different CPs in their capsid (31). Whether these viruses use two different CPs in their capsid (as some RNA viruses do), or whether these are intermediates in the exchange of CP genes, as predicted from the gene capture mechanism proposed by Stedman (2013) (18), is unclear.…”

Section: Crucivirus Capsid Protein (Cp)mentioning

confidence: 99%

“…It was hypothesized that this virus originated by the acquisition of a capsid gene from an RNA virus through a yet to be demonstrated RNA-DNA recombination event (15,18). Since the discovery of this putatively "chimeric virus", 80 circular sequences encoding a Rep and a CP that share homology to tombusvirus CPs have been found in different environments around the globe (19,20,(29)(30)(31)(21)(22)(23)(24)(25)(26)(27)(28). This growing group of viruses have been branded "cruciviruses", as they imply the crossing between CRESS-DNA viruses and RNA tombusviruses (27).…”

Section: Introductionmentioning

confidence: 99%

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Unveiling Crucivirus Diversity by Mining Metagenomic Data

Higuera

Kasun

Torrance

et al. 2020

Preprint

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The discovery of cruciviruses revealed the most explicit example of a common protein homologue between DNA and RNA viruses to date. Cruciviruses are a novel group of circular Rep-encoding ssDNA (CRESS-DNA) viruses that encode capsid proteins (CPs) that are most closely related to those encoded by RNA viruses in the family Tombusviridae. The apparent chimeric nature of the two core proteins encoded by crucivirus genomes suggests horizontal gene transfer of CP genes between DNA and RNA viruses. Here, we identified and characterized 451 new crucivirus genomes and ten CP-encoding circular genetic elements through de novo assembly and mining of metagenomic data. These genomes are highly diverse, as demonstrated by sequence comparisons and phylogenetic analysis of subsets of the protein sequences they encode.Most of the variation is reflected in the replication associated protein (Rep) sequences, and much of the sequence diversity appears to be due to recombination. Our results suggest that recombination tends to occur more frequently among groups of cruciviruses with relatively similar capsid proteins, and that the exchange of Rep protein domains between cruciviruses is rarer than gene exchange. Altogether, we provide a comprehensive and descriptive characterization of cruciviruses. IMPORTANCEViruses are the most abundant biological entities on Earth. In addition to their impact on animal and plant health, viruses have important roles in ecosystem dynamics as well as in the evolution of the biosphere. Circular Rep-encoding single-stranded (CRESS) DNA viruses are ubiquitous in nature, many are agriculturally important, and are viruses that appear to have multiple origins from prokaryotic plasmids. CRESS-DNA viruses such as the cruciviruses, have homologues of capsid proteins (CPs) encoded by RNA viruses. The genetic structure of cruciviruses attests to the transfer of capsid genes between disparate groups of viruses. However, the evolutionary history of cruciviruses is still unclear. By collecting and analyzing cruciviral sequence data, we provide a deeper insight into the evolutionary intricacies of cruciviruses. Our results reveal an unexpected diversity of this virus group, with frequent recombination as an important determinant of variability. Bootstrap support 0.95 -1 0.8 -0.95 1 subs/site UF Bootstrap support 0.95 -1 0.8 -0.95 1 subs/site Rep CP A B * Endonuclease Helicase UF Bootstrap support 0.95 -1 0.8 -0.95 Cp-based clusters Endonuclease Helicase UF Bootstrap support 0.95 -1 0.8 -0.95 Endonuclease Helicase UF Bootstrap support 0.95 -1 0.8 -0.95

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Discovery of several thousand highly diverse circular DNA viruses

Cited by 156 publications

References 100 publications

Prokaryotic and Viral Community Composition of Freshwater Springs in Florida, USA

Prokaryotic and Viral Community Composition of Freshwater Springs in Florida, USA

A high-resolution map of bacteriophage øX174 transcription

Unveiling Crucivirus Diversity by Mining Metagenomic Data

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