Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean

Kaneko, Hiroto; Blanc-Mathieu, Romain; Endo, Hisashi; Chaffron, Samuel; Delmont, Tom O.; Gaïa, Morgan; Henry, Nicolas; Hernández-Velázquez, Rodrigo; Nguyen, Canh Hao; Mamitsuka, Hiroshi; Forterre, Patrick; Jaillon, Olivier; Vargas, Colomban de; Sullivan, Matthew B.; Suttle, Curtis A.; Guidi, Lionel; Ogata, Hiroyuki

doi:10.1016/j.isci.2020.102002

Cited by 50 publications

(43 citation statements)

References 66 publications

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“…The effect that viruses have on their hosts’ ecological roles depends on their mode of infection. Lytic predator–prey interactions can control bacterial population densities and regulate the rate of biomass and organic matter transformations [ 26 , 27 ]. In temperate interactions such as lysogeny, the phage integrates into the host’s genome as a prophage or replicates as an extrachromosomal element [ 28 , 29 ].…”

Section: Introductionmentioning

confidence: 99%

Prophage Genomics and Ecology in the Family Rhodobacteraceae

et al. 2021

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Roseobacters are globally abundant bacteria with critical roles in carbon and sulfur biogeochemical cycling. Here, we identified 173 new putative prophages in 79 genomes of Rhodobacteraceae. These prophages represented 1.3 ± 0.15% of the bacterial genomes and had no to low homology with reference and metagenome-assembled viral genomes from aquatic and terrestrial ecosystems. Among the newly identified putative prophages, 35% encoded auxiliary metabolic genes (AMGs), mostly involved in secondary metabolism, amino acid metabolism, and cofactor and vitamin production. The analysis of integration sites and gene homology showed that 22 of the putative prophages were actually gene transfer agents (GTAs) similar to a GTA of Rhodobacter capsulatus. Twenty-three percent of the predicted prophages were observed in the TARA Oceans viromes generated from free viral particles, suggesting that they represent active prophages capable of induction. The distribution of these prophages was significantly associated with latitude and temperature. The prophages most abundant at high latitudes encoded acpP, an auxiliary metabolic gene involved in lipid synthesis and membrane fluidity at low temperatures. Our results show that prophages and gene transfer agents are significant sources of genomic diversity in roseobacter, with potential roles in the ecology of this globally distributed bacterial group.

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Section: Introductionmentioning

confidence: 99%

Prophage Genomics and Ecology in the Family Rhodobacteraceae

et al. 2021

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“…Some early studies were prescient in suggesting that these viruses are a diverse and underappreciated component of viral diversity in the ocean ( 27 – 30 ). More recent work has confirmed this view and revealed that a diverse range of Nucleocytoviricota inhabit the global ocean and likely contribute to key processes such as algal bloom termination and carbon export ( 12 , 31 – 36 ). Some metatranscriptomic studies have also begun to note the presence of Nucleocytoviricota transcripts in marine samples, confirming their activity ( 37 – 39 ).…”

Section: Introductionmentioning

confidence: 82%

High Transcriptional Activity and Diverse Functional Repertoires of Hundreds of Giant Viruses in a Coastal Marine System

Moniruzzaman

Aylward

2021

mSystems

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“…Phylogeny-guided filtering of host predictions and its assessment. We developed Taxon Interaction Mapper (TIM) to improve host predictions by co-occurrence approaches (35). TIM assumes that evolutionarily related viruses tend to infect evolutionarily related hosts (18,74) and extract the most likely virus-host associations from the co-occurrence networks.…”

Section: Methodsmentioning

confidence: 99%

Quantitative Assessment of Nucleocytoplasmic Large DNA Virus and Host Interactions Predicted by Co-occurrence Analyses

Meng

Endo

Blanc-Mathieu

et al. 2021

mSphere

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Nucleocytoplasmic large DNA viruses (NCLDVs) are highly diverse and abundant in marine environments. However, the knowledge of their hosts is limited because only a few NCLDVs have been isolated so far. Taking advantage of the recent large-scale marine metagenomics census, in silico host prediction approaches are expected to fill the gap and further expand our knowledge of virus-host relationships for unknown NCLDVs. In this study, we built co-occurrence networks of NCLDVs and eukaryotic taxa to predict virus-host interactions using Tara Oceans sequencing data. Using the positive likelihood ratio to assess the performance of host prediction for NCLDVs, we benchmarked several co-occurrence approaches and demonstrated an increase in the odds ratio of predicting true positive relationships 4-fold compared to random host predictions. To further refine host predictions from high-dimensional co-occurrence networks, we developed a phylogeny-informed filtering method, Taxon Interaction Mapper, and showed it further improved the prediction performance by 12-fold. Finally, we inferred virophage-NCLDV networks to corroborate that co-occurrence approaches are effective for predicting interacting partners of NCLDVs in marine environments. IMPORTANCE NCLDVs can infect a wide range of eukaryotes, although their life cycle is less dependent on hosts compared to other viruses. However, our understanding of NCLDV-host systems is highly limited because few of these viruses have been isolated so far. Co-occurrence information has been assumed to be useful to predict virus-host interactions. In this study, we quantitatively show the effectiveness of co-occurrence inference for NCLDV host prediction. We also improve the prediction performance with a phylogeny-guided method, which leads to a concise list of candidate host lineages for three NCLDV families. Our results underpin the usage of co-occurrence approaches for the metagenomic exploration of the ecology of this diverse group of viruses.

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Eukaryotic virus composition can predict the efficiency of carbon export in the global ocean

Cited by 50 publications

References 66 publications

Prophage Genomics and Ecology in the Family Rhodobacteraceae

Prophage Genomics and Ecology in the Family Rhodobacteraceae

High Transcriptional Activity and Diverse Functional Repertoires of Hundreds of Giant Viruses in a Coastal Marine System

Quantitative Assessment of Nucleocytoplasmic Large DNA Virus and Host Interactions Predicted by Co-occurrence Analyses

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