Unveiling Crucivirus Diversity by Mining Metagenomic Data

Higuera, Ignacio de la; Kasun, George W.; Torrance, Ellis L.; Pratt, Alyssa A.; Maluenda, Amberlee; Colombet, Jonathan; Bisseux, Maxime; Ravet, Viviane; Dayaram, Anisha; Stainton, Daisy; Kraberger, Simona; Zawar-Reza, Peyman; Goldstien, Sharyn J.; Briskie, James V.; White, Robyn; Taylor, Helen R.; Gomez, Christopher; Ainley, David G.; Harding, Jon S.; Fontenele, Rafaela S.; Schreck, Joshua; Ribeiro, S. G.; Oswald, Stephen A.; Arnold, Jennifer M.; Enault, François; Varsani, Arvind; Stedman, Kenneth M.

doi:10.1101/2020.02.27.967703

Cited by 6 publications

(7 citation statements)

References 102 publications

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“…This indicates that the dinoRNAV mcp sequences reported here constitute exogenous viral infections, rather than endogenous viral elements (EVEs; [62]) within their host's genome. Considering that the gene amplicons reported here were generated from unfractionated coral tissue, dinoRNAV mcp detections in this study could potentially arise from four sources: RNA genomes within intact dinoRNAV capsids (sensu [29]); mcp genes that are being expressed in host cells during a dinoRNAV replication cycle; free dinoRNAV genomes that may occur as extrachromosomal RNA in a latent [26] or carrier state similar to pseudolysogeny [82,83]; and /or chimeric RNA viruses with analogous mcp gene sequences [61]. However, the identification of highly abundant transcripts with homology to Symbiodiniaceae-associated dinoRNAV RdRp genes in the metatranscriptomes (Table S2, S3) indicates that mcp gene amplicons in this study are most parsimoniously interpreted as derived from dinoRNAVs [79,80].…”

Section: Healthy Corals Contain Millions Of Symbiodiniaceae Cells Per CM 2 Of Coral Tissue; Our Resultsmentioning

confidence: 99%

Thermal stress triggers productive viral infection of a key coral reef symbiont

Grupstra

Howe‐Kerr

Veglia

et al. 2021

Preprint

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Climate change-driven ocean warming is increasing the frequency and severity of bleaching events, in which corals appear whitened after losing their dinoflagellate endosymbionts (family Symbiodiniaceae). Viral infections of Symbiodiniaceae may contribute to some bleaching signs, but little empirical evidence exists to support this hypothesis. We present the first temporal analysis of a viral lineage—the Symbiodiniaceae-infecting ‘dinoRNAVs’—in coral colonies exposed to a 5-day heat treatment. Throughout the experiment, all colonies were dominated by Symbiodiniaceae in the genus Cladocopium, but 124 dinoRNAV major capsid protein ‘aminotypes’ (unique amino acid sequences) were detected across coral genets and treatments. Seventeen dinoRNAV aminotypes were found only in heat-treated fragments, and 22 aminotypes were detected at higher relative abundances in heat-treated fragments. DinoRNAVs also exhibited higher alpha diversity and dispersion under heat stress. Together, these findings provide the first empirical evidence that exposure to high temperatures triggers some dinoRNAVs to switch from a persistent to a productive infection mode within heat-stressed corals. Over extended time frames, we hypothesize that cumulative dinoRNAV lysis of Symbiodiniaceae cells during productive infections could decrease Symbiodiniaceae densities within corals, observable as bleaching signs. This study sets the stage for reef-scale investigations of dinoRNAV dynamics during bleaching events.

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Section: Healthy Corals Contain Millions Of Symbiodiniaceae Cells Per CM 2 Of Coral Tissue; Our Resultsmentioning

confidence: 99%

Thermal stress triggers productive viral infection of a key coral reef symbiont

Grupstra

Howe‐Kerr

Veglia

et al. 2021

Preprint

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“…In general, for viruses in the phylum Cressdnaviricota , the CPs are more diverse than the Reps. Furthermore, the CPs of geminiviruses share homology to those of albetoviruses (linear ssRNA(+) genomes) [ 65 ], and a group of unclassified cressdnavirues have CPs that are homologous to those of tombusviruses (linear ssRNA(+) genomes) [ 64 , 66 , 67 , 68 ].…”

Section: Resultsmentioning

confidence: 99%

“…The Reps identified in this study are highlighted in green and relevant clades of the tree are shown in the expanded view. Sequences with taxa names CruV-203, -227, -319, and -320 are from metagenomic derived sequences reported in de la Higuera et al [ 64 ] and do not have accession #s assigned. The level of branch support (>0.8) is depicted as different sized shaded circles.…”

Section: Figurementioning

confidence: 99%

Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula

Levy

Fontenele

Harding

et al. 2020

Viruses

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There is growing interest in uncovering the viral diversity present in wild animal species. The remote Antarctic region is home to a wealth of uncovered microbial diversity, some of which is associated with its megafauna, including penguin species, the dominant avian biota. Penguins interface with a number of other biota in their roles as marine mesopredators and several species overlap in their ranges and habitats. To characterize the circular single-stranded viruses related to those in the phylum Cressdnaviricota from these environmental sentinel species, cloacal swabs (n = 95) were obtained from King Penguins in South Georgia, and congeneric Adélie Penguins, Chinstrap Penguins, and Gentoo Penguins across the South Shetland Islands and Antarctic Peninsula. Using a combination of high-throughput sequencing, abutting primers-based PCR recovery of circular genomic elements, cloning, and Sanger sequencing, we detected 97 novel sequences comprising 40 ssDNA viral genomes and 57 viral-like circular molecules from 45 individual penguins. We present their detection patterns, with Chinstrap Penguins harboring the highest number of new sequences. The novel Antarctic viruses identified appear to be host-specific, while one circular molecule was shared between sympatric Chinstrap and Gentoo Penguins. We also report viral genotype sharing between three adult-chick pairs, one in each Pygoscelid species. Sequence similarity network approaches coupled with Maximum likelihood phylogenies of the clusters indicate the 40 novel viral genomes do not fall within any known viral families and likely fall within the recently established phylum Cressdnaviricota based on their replication-associated protein sequences. Similarly, 83 capsid protein sequences encoded by the viruses or viral-like circular molecules identified in this study do not cluster with any of those encoded by classified viral groups. Further research is warranted to expand knowledge of the Antarctic virome and would help elucidate the importance of viral-like molecules in vertebrate host evolution.

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“…Evolutionary analysis of microphage genomes assembled from public virome sequences indicates that coinfection events may have primed genetic exchange between ssDNA or dsDNA viruses (146). Metagenomic studies that uncovered chimeric RNA-DNA hybrid viruses imply that systematic coinfections have played crucial roles in the ecology and evolution of these viruses (147,148). For example, evaluation of 13,103 viruses from 6,564 microbial hosts in three distinct large-scale microbial data sets predicted that host ecology and VVIs strongly regulate frequency and extent of viral coinfections (149) (Figure 4).…”

Section: Spontaneousmentioning

confidence: 99%

Integrating Viral Metagenomics into an Ecological Framework

et al. 2021

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Viral metagenomics has expanded our knowledge of the ecology of uncultured viruses, within both environmental (e.g., terrestrial and aquatic) and host-associated (e.g., plants and animals, including humans) contexts. Here, we emphasize the implementation of an ecological framework in viral metagenomic studies to address questions in virology rarely considered ecological, which can change our perception of viruses and how they interact with their surroundings. An ecological framework explicitly considers diverse variants of viruses in populations that make up communities of interacting viruses, with ecosystem-level effects. It provides a structure for the study of the diversity, distributions, dynamics, and interactions of viruses with one another, hosts, and the ecosystem, including interactions with abiotic factors. An ecological framework in viral metagenomics stands poised to broadly expand our knowledge in basic and applied virology. We highlight specific fundamental research needs to capitalize on its potential and advance the field. Expected final online publication date for the Annual Review of Virology, Volume 8 is September 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

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Unveiling Crucivirus Diversity by Mining Metagenomic Data

Cited by 6 publications

References 102 publications

Thermal stress triggers productive viral infection of a key coral reef symbiont

Thermal stress triggers productive viral infection of a key coral reef symbiont

Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula

Integrating Viral Metagenomics into an Ecological Framework

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