IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes

Páez-Espino, David; Roux, Simon; Chen, I-Min A.; Palaniappan, Krishna; Ratner, Anna; Chu, Ken; Huntemann, Marcel; Reddy, T. B. K.; Pons, Joan Carles; Llabrés, Mercè; Eloe‐Fadrosh, Emiley A.; Ivanova, Natalia; Kyrpides, Nikos C.

doi:10.1093/nar/gky1127

Cited by 161 publications

(200 citation statements)

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“…We used the host taxonomic information derived from IMG/VR version 1.0 where two computational approaches were used: (1) host assignment based on virus clusters that included isolate virus genomes with known hosts and (2) CRISPR-spacer sequence matches (only tolerating 1 SNP over the whole spacer length as cutoffs). To further complement the host assignment from IMG/VR version 1.0, we used a classification of the viral protein families (used in the virus identification pipeline) to determine the domain (Eukaryotic, Bacterial, or Archaeal) of the host predicted for 85.6% of the viral sequences described in Paez-Espino et al 40 ( Supplementary Table 3). Briefly, the viral protein families were benchmarked against the viral RefSeq genomes and the viral genomes with predicted host from the prokaryotic virus of orthologous groups database 50 obtaining a subset of them used as host-type marker genes.…”

Section: Methodsmentioning

confidence: 99%

“…2 and 3) and these contigs were primarily from vegetated biomes (Extended Data Tables 2 and 3). Also, when analyzing the entire IMG/VR virus database 40 , viral chitosanases were exclusively found in soil or freshwater viruses (66% vs. 33% of the cases, respectively). This finding highlights the potential importance of viral-encoded chitosanase functions in bacteria in ecosystems where chitin is abundant.…”

Section: A New Paradigm: Cross-domain Transfer Of Biogeochemical Funcmentioning

confidence: 99%

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Untapped viral diversity in global soil metagenomes

Graham

Páez-Espino

Brislawn

et al. 2019

Preprint

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Viruses outnumber every other biological entity on Earth, and soil viruses are particularly diverse compared to other habitats. However, we have limited understanding of soil viruses because of the tremendous variation in soil ecosystems and because of the lack of appropriate screening tools. Here, we determined the global distribution of more than 24,000 soil viral sequences and their potential hosts, including >1,600 sequences associated with giant viruses. The viral sequences, derived from 668 terrestrial metagenomes, greatly extend existing knowledge of soil viral diversity and viral biogeographical distribution. We screened these sequences to identify a suite of cosmopolitan auxiliary metabolic genes (AMGs) encoding enzymes involved in soil organic carbon decomposition across soil biomes. Additionally, we provide evidence for viral facilitation of multi-domain linkages in soils by locating a fungal chitosanase in bacteriophages, generating a new paradigm of how viruses can serve as exchange vectors of carbon metabolism across domains of life.

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Section: Methodsmentioning

confidence: 99%

Section: A New Paradigm: Cross-domain Transfer Of Biogeochemical Funcmentioning

confidence: 99%

Untapped viral diversity in global soil metagenomes

Graham

Páez-Espino

Brislawn

et al. 2019

Preprint

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“…Likewise, we did not find evidence of this gene in Amorphea 230 (which includes Amoebozoa, animals, fungi, and related protists). Although these initial results 231 implied a distribution that might be truly restricted to green plants (Viridiplantae), searches of other 232 major eukaryotic lineages found that plant-like MSH1 homologs carrying the characteristic GIY-YIG and another gammaproteobacterium of uncertain classification, as well as some unclassified viruses curated from environmental and metagenomic datasets (42,43). Phylogenetic analysis confirmed (24,48,49).…”

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confidence: 99%

“…To further 708 expand our search to include some of the vast amount of biological diversity that is unculturable and 709 only detected in environmental samples, we queried a sample of 2000 metagenome assemblies 710 from the JGI IMG/MER repository (43). We also searched against the IMG/VR database, which 711 houses the largest available collection of viral sequences from both sequenced isolates and 712 environmental samples (42). In cases where MSH1-like sequences were identified on metagenomic 713 scaffolds, we searched other proteins encoded in the flanking sequence against the NCBI nr 714 database to infer possible origins for the scaffold.…”

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confidence: 99%

MSH1 is required for maintenance of the low mutation rates in plant mitochondrial and plastid genomes

Waneka

Broz

et al. 2020

Preprint

101

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2Mitochondrial and plastid genomes in land plants exhibit some of the slowest rates of sequence 3 evolution observed in any eukaryotic genome, suggesting an exceptional ability to prevent or correct 4 mutations. However, the mechanisms responsible for this extreme fidelity remain unclear. We tested 5 seven candidate genes involved in cytoplasmic DNA replication, recombination, and repair (POLIA, 6 POLIB, MSH1, RECA3, UNG, FPG, and OGG1) for effects on mutation rates in the model 7 angiosperm Arabidopsis thaliana by applying a highly accurate DNA sequencing technique (duplex 8 sequencing) that can detect newly arisen mitochondrial and plastid mutations still at low 9 heteroplasmic frequencies. We find that disrupting MSH1 (but not the other candidate genes) leads 10 to massive increases in the frequency of point mutations and small indels and changes to the 11 mutation spectrum in mitochondrial and plastid DNA. We also used droplet digital PCR to show 12 transmission of de novo heteroplasmies across generations in msh1 mutants, confirming a 13 contribution to heritable mutation rates. This dual-targeted gene is part of an enigmatic lineage within 14 the mutS mismatch repair family that we find is also present outside of green plants in multiple 15 eukaryotic groups (stramenopiles, alveolates, haptophytes, and cryptomonads), as well as certain 16 bacteria and viruses. MSH1 has previously been shown to limit ectopic recombination in plant 17 cytoplasmic genomes. Our results point to a broader role in recognition and correction of errors in 18 plant mitochondrial and plastid DNA sequence, leading to greatly suppressed mutation rates 19 perhaps via initiation of double-stranded breaks and repair pathways based on faithful homologous 20 recombination.It has been apparent for more than 30 years that rates of nucleotide substitution in plant 24 mitochondrial and plastid genomes are unusually low (1,2). In angiosperms, mitochondrial and 25 plastid genomes have synonymous substitution rates that are on average approximately 16-fold and 26 5-fold slower than the nucleus, respectively (3). The fact that these low rates are evident even at 27 sites that are subject to relatively small amounts of purifying selection (4, 5) suggests that they are 28 the result of very low underlying mutation rates -a surprising observation especially when 29 contrasted with the rapid accumulation of mitochondrial mutations in many eukaryotic lineages (6,7). 30Although the genetic mechanisms that enable plants to achieve such faithful replication and 31 transmission of cytoplasmic DNA sequences have not been determined, a number of hypotheses 32 can be envisioned. One possibility is that the DNA polymerases responsible for replicating 33 mitochondrial and plastid DNA (8) might have unusually high fidelity. However, in vitro assays with 34 the two partially redundant bacterial-like organellar DNA polymerases in Arabidopsis thaliana, PolIA 35(At1g50840) and PolIB (At3g20540), have indicated that they are highly error-prone (9), with 36 misincorpo...

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“…The largest oral virome study was conducted in 2015, which generated and analyzed more than 100 Gb shotgun sequencing data from 25 samples (20 dental plaque specimens and 5 salivary) to primarily explore the phage-bacteria interaction network (12). More recently, shotgun metagenome sequencing of 3,042 samples from various environments, including the human oral cavity, was conducted in a project aimed at uncovering the Earth’s virome (13), which achieved an almost 3-fold increase in the metagenome samples (14). Re-analysis of the Earth’s virome data revealed signatures of genetic conflict invoked by the coevolution of phages and host oral bacteria enriched in the human oral cavity (15), suggesting it as an attractive system to study coevolution using metagenomic data.…”

Section: Introductionmentioning

confidence: 99%

Long-read shotgun metagenome sequencing using PromethION uncovers novel bacteriophages, their abundance, and interaction with host bacterial immunity in the oral microbiota

Yahara

Suzuki

Hirabayashi

et al. 2020

Preprint

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17 18 Bacteriophages (phages), or bacterial viruses, are very diverse and highly abundant worldwide, 19 including human microbiomes. Although a few metagenomic studies have focused on oral 20 phages, they relied on short-read sequencing. Here, we conducted a long-read metagenomic 21 study of human saliva for the first time using PromethION that requires a smaller amount of 22 DNA than PacBio. Our analyses, which integrated both PromethION and HiSeq data of >30 Gb 23 per sample, revealed N50 ranging from 187-345 kb and thousands of contigs with >1 kb 24 accounting for > 99% of all contigs on which 94-96% of HiSeq reads were mapped. We 25 identified hundreds of viral contigs (95 phages and 333 prophages on an average per sample); 26 0-43.8% and 12.5-56.3% of the "most confident" phages and prophages, respectively, didn't 27 cluster with those reported previously and were identified as novel. Our integrated analyses 28 identified highly abundant oral phages/prophages, including a novel Streptococcus phage 29 cluster and nine jumbo phages/prophages. Interestingly, 86% of the phage cluster and 67% of 30 the jumbo phages/prophages contained remote homologs of antimicrobial resistance genes, 31 suggesting their potential role as a source of recombination to generate new resistance genes. 32Pan-genome analysis of the phages/prophages revealed remarkable diversity, identifying 0.3% 33 and 86.4% of the genes as core and singletons, respectively. Functional annotation revealed 34 that the highest fraction of the core genes was enriched in phage morphogenesis, followed by 35 the fraction enriched in host cellular processes. Furthermore, our study suggested that oral 36 phages present in human saliva are under selective pressure for escaping CRISPR immunity. 37 (250/250 words) 38 39 Importance 40 41Despite the abundance and grave implications oral bacterial viruses in health and disease, little 42 is known regarding the different groups of oral bacterial viruses, their relative abundances 43 under various conditions, and their activities. We provided answers to these questions for the first time utilizing a recently developed sequencer that can capture and sequence long DNA 45 fragments, including viruses, and requires only a small amount of DNA input, making it 46 suitable for analyzing human oral samples. We identified hundreds of viral sequences, 47 (147/150 words) 54 55

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IMG/VR v.2.0: an integrated data management and analysis system for cultivated and environmental viral genomes

Cited by 161 publications

References 33 publications

Untapped viral diversity in global soil metagenomes

Untapped viral diversity in global soil metagenomes

MSH1 is required for maintenance of the low mutation rates in plant mitochondrial and plastid genomes

Long-read shotgun metagenome sequencing using PromethION uncovers novel bacteriophages, their abundance, and interaction with host bacterial immunity in the oral microbiota

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