A comprehensive and quantitative exploration of thousands of viral genomes

Mahmoudabadi, Gita; Phillips, Rob

doi:10.7554/elife.31955

Cited by 73 publications

(78 citation statements)

References 70 publications

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“…The GC content of the 183 LBVGs ranged from 29.1 to 66.7%, and all genome sizes were <120 kb except for LBVG_1 (318 kb) and LBVG_2 (190 kb) ( Fig. 1A), which were within the range of known prokaryotic dsDNA viral genomes (Mahmoudabadi and Phillips, 2018).…”

Section: Overview Of Samples and Assembliesmentioning

confidence: 60%

“…prokaryotic dsDNA viral genomes (73,74). Functional annotation of open reading frames (ORFs) demonstrated that 177 of the 183 LBVGs contained a terminase large subunit gene, and 181 LBVGs had one or more tailed-virus hallmark genes (i.e., terminase, tail, capsid or portal), indicating that they were bona fide viral genomes.…”

Section: Overview Of Samples and Assembliesmentioning

confidence: 99%

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Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake

Okazaki

Nishimura

Yoshida

et al. 2019

Preprint

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The use of metagenomics has dramatically expanded the known virosphere, but freshwater viral diversity and the ecological relationships between viruses and hosts remain poorly understood. In this study, we conducted a large-scale metagenomic exploration of planktonic dsDNA prokaryotic viruses by sequencing both virion (<0.22 μm) and cellular (0.22-5.0 μm) fractions collected spatiotemporally from a deep freshwater lake (Lake Biwa, Japan). This simultaneously reconstructed 183 complete (i.e., circular) viral genomes and 57 bacterioplankton metagenome-assembled genomes. Spatiotemporal, intra-and extra-cellular dynamics of individual viruses assessed through metagenomic read coverage revealed a hypolimnion-specific viral community analogous to the vertically-stratified bacterioplankton community. The hypolimnetic community was generally stable during stratification, but occasionally shifted abruptly due to lysogenic induction, presumably reflecting low bacterial productivity in the hypolimnion. Genes involved in assimilatory sulfate reduction were encoded in 20 (10.9%) viral genomes, including those of dominant viruses, and may aid viral propagation in sulfurlimited freshwater systems. Hosts were predicted for 40 (21.9%) viral genomes, encompassing 10 phyla (or classes of Proteobacteria) including ubiquitous freshwater bacterioplankton lineages (e.g., LD12 and Ca. Nitrosoarchaeum). Comparison with published metagenomes revealed phylogeographic connectivity of viral communities in geographically isolated habitats, probably following the phylogeographic connectivity of their hosts. Notably, analogous to their hosts, actinobacterial viruses were among the most diverse, ubiquitous, and abundant viral groups in freshwater systems, with high lytic replication rates in surface waters. This result suggested that freshwater Actinobacteria are under high viral lytic pressure, which likely facilitated their genomic micro-diversification to elude viral recognition. Significance StatementMetagenomics allows for the reconstruction of bacterial and viral genomes without cultivation, contributing substantially to elucidation of bacterial and viral diversity and their key ecological roles.In this study, we report the largest-scale metagenomic exploration of freshwater prokaryotic viruses to date. We investigated the hypolimnion of a deep freshwater lake and tracked viruses throughout their life cycles, including both intra-and extra-cellular phases. This method allowed us to reconstruct both viral and host genomes and characterize numerous novel virus-host interactions, including those involving ubiquitous freshwater bacterial lineages. When the data were compared with published metagenomic datasets, we uncovered genome-resolved phylogeographic connectivity among viruses from geographically isolated habitats and identified ecologically important viral groups that are ubiquitous in aquatic habitats.In total, 12 water samples were collected at a pelagic site on Lake Biwa, the largest freshwater lake in Japan. The epilimnion (5 m) was ...

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Section: Overview Of Samples and Assembliesmentioning

confidence: 60%

Section: Overview Of Samples and Assembliesmentioning

confidence: 99%

Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake

Okazaki

Nishimura

Yoshida

et al. 2019

Preprint

View full text Add to dashboard Cite

show abstract

“…The guanine-cytosine (GC) content of the 183 LBVGs ranged from 29.1% to 66.7%, and all genome sizes were < 120 kb except for LBVG_1 (318 kb) and LBVG_2 (190 kb) ( Fig. 1A), which were within the range of known prokaryotic dsDNA viral genomes (Mahmoudabadi and Phillips, 2018).…”

Section: Overview Of Samples and Assembliesmentioning

confidence: 82%

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

Okazaki

Nishimura

Yoshida

et al. 2019

Environmental Microbiology

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Summary Metagenomics has dramatically expanded the known virosphere, but freshwater viral diversity and their ecological interaction with hosts remain poorly understood. Here, we conducted a metagenomic exploration of planktonic dsDNA prokaryotic viruses by sequencing both virion (<0.22 μm) and cellular (0.22–5.0 μm) fractions collected spatiotemporally from a deep freshwater lake (Lake Biwa, Japan). This simultaneously reconstructed 183 complete (i.e., circular) viral genomes and 57 bacterioplankton metagenome‐assembled genomes. Analysis of metagenomic read coverage revealed vertical partitioning of the viral community analogous to the vertically stratified bacterioplankton community. The hypolimnetic community was generally stable during stratification, but occasionally shifted abruptly, presumably due to lysogenic induction. Genes involved in assimilatory sulfate reduction were encoded in 20 (10.9%) viral genomes, including those of dominant viruses, and may aid viral propagation in sulfur‐limited freshwater systems. Hosts were predicted for 40 (21.9%) viral genomes, encompassing 10 phyla (or classes of Proteobacteria) including ubiquitous freshwater bacterioplankton lineages (e.g., Ca. Fonsibacter and Ca. Nitrosoarchaeum). Comparison with viral genomes derived from published metagenomes revealed viral phylogeographic connectivity in geographically isolated habitats. Notably, analogous to their hosts, actinobacterial viruses were among the most diverse, ubiquitous and abundant viral groups in freshwater systems, with potential high lytic activity in surface waters.

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“…). The context is clearly prophage‐like because the gene constellation from terminase to tail fibre resembles the classic lambdoid Caudovirales (double‐stranded DNA tailed prophages) structure previously observed in bacteria, including Gram‐positive Firmicutes (Desiere et al ., ; Lucchini et al ., ; Brüssow and Desiere, ; Canchaya et al ., ; Cardarelli et al ., ; Pope et al ., ; Mahmoudabadi and Phillips, ). Specifically, we annotated the following modules: (i) Replication unit with helicase and primase.…”

Section: Resultsmentioning

confidence: 99%

ACI‐1 beta‐lactamase is widespread across human gut microbiomes in Negativicutes due to transposons harboured by tailed prophages

Rands

Starikova

Brüssow

et al. 2018

Environmental Microbiology

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Antibiotic resistance is increasing among pathogens, and the human microbiome contains a reservoir of antibiotic resistance genes. Acidaminococcus intestini is the first Negativicute bacterium (Gram-negative Firmicute) shown to be resistant to beta-lactam antibiotics. Resistance is conferred by the aci1 gene, but its evolutionary history and prevalence remain obscure. We discovered that ACI-1 proteins are phylogenetically distinct from beta-lactamases of Gram-positive Firmicutes and that aci1 occurs in bacteria scattered across the Negativicute clade, suggesting lateral gene transfer. In the reference A. intestini RyC-MR95 genome, we found transposons residing within a tailed prophage context are likely vehicles for aci1's mobility. We found aci1 in 56 (4.4%) of 1,267 human gut metagenomes, mostly hosted within A. intestini, and, where could be determined, mostly within a consistent mobile element constellation. These samples are from Europe, China and the USA, showing that aci1 is distributed globally. We found that for most Negativicute assemblies with aci1, the prophage observed in A. instestini is absent, but in all cases aci1 is flanked by varying transposons. The chimeric mobile elements we identify here likely have a complex evolutionary history and potentially provide multiple complementary mechanisms for antibiotic resistance gene transfer both within and between cells.

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A comprehensive and quantitative exploration of thousands of viral genomes

Cited by 73 publications

References 70 publications

Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake

Genome-resolved viral and cellular metagenomes revealed potential key virus-host interactions in a deep freshwater lake

Genome‐resolved viral and cellular metagenomes revealed potential key virus‐host interactions in a deep freshwater lake

ACI‐1 beta‐lactamase is widespread across human gut microbiomes in Negativicutes due to transposons harboured by tailed prophages

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