Biogeography of marine giant viruses reveals their interplay with eukaryotes and ecological functions

Endo, Hisashi; Blanc-Mathieu, Romain; Li, Yanze; Salazar, Guillem; Henry, Nicolas; Labadie, Karine; Vargas, Colomban de; Sullivan, Matthew B.; Bowler, Chris; Wincker, Patrick; Karp‐Boss, Lee; Sunagawa, Shinichi; Ogata, Hiroyuki

doi:10.1038/s41559-020-01288-w

Cited by 103 publications

(120 citation statements)

References 73 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…This was expected given the high abundance and diversity of NCLDVs in marine environments (18,21) and the identification of HGT between these viruses and diverse eukaryotic lineages (24). The networks were dominated by the Mimiviridae nodes, which is consistent with previous reports that Mimiviridae is the most abundant and has the widest array of transcribed genes out of NCLDV families in marine environments (22,23). Mimiviridae was known to infect amoebae, algae, and stramenopiles (3).…”

Section: Discussionsupporting

confidence: 85%

“…Type B DNA polymerase (polB) was used as the marker gene for NCLDVs. A total of 6818 NCLDV polB OTUs were extracted from the metagenomic datasets (i.e., the second version of the Ocean Microbial Reference Gene Catalog, OM-RGC.v2) using the pplacer phylogenetic placement method (ML tree) (22,60,61). These polB sequences were classified into seven NCLDV families (Mimiviridae, Phycodnaviridae, Marseilleviridae, Ascoviridae, Iridoviridae, Asfarviridae, and Poxviridae) and two other giant virus groups ("Medusaviridae" and "Pithoviridae").…”

Section: Metagenomic and Metabarcoding Datamentioning

confidence: 99%

See 1 more Smart Citation

Quantitative assessment of NCLDV–host interactions predicted by co-occurrence analyses

Meng

Endo

Blanc-Mathieu

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

Nucleocytoplasmic DNA viruses (NCLDVs) are highly diverse and abundant in marine environments. However, knowledge of their hosts is limited because only a few NCLDVs have been isolated. By taking advantage of the rapidly increasing metagenomic data, in silico host prediction approaches are expected to fill this gap between known virus-host relationships and the true but largely unknown amount of NCLDVs. In this study, we built co-occurrence networks between NCLDVs and eukaryotes using the Tara Oceans metagenome and metabarcoding datasets to predict virus-host interactions. Using the positive likelihood ratio to assess the performance of host prediction for NCLDVs, we demonstrated that co-occurrence approaches can increase the odds of predicting true positive relationships four-fold compared with random host predictions in the high-weight region (weight > 0.4). To refine the host predictions from high-dimensional co-occurrence networks, we employed a recently proposed phylogeny-based method, Taxon Interaction Mapper, and showed that Taxon Interaction Mapper further improved the prediction performance eight-fold using weight cut-off filtration (> 0.4). Finally, we inferred virophage and NCLDV networks that further corroborated that co-occurrence approaches are effective for predicting NCLDV hosts in marine environments.

show abstract

Section: Discussionsupporting

confidence: 85%

Section: Metagenomic and Metabarcoding Datamentioning

confidence: 99%

Quantitative assessment of NCLDV–host interactions predicted by co-occurrence analyses

Meng

Endo

Blanc-Mathieu

et al. 2020

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…While most cultured Asfarviruses were isolated from sewage samples, various metagenomic studies have revealed that NCLDVs are highly diverse and abundant in aquatic environments (Monier et al, 2008; Hingamp et al, 2013), and one recent study noted that Asfarviruses are prevalent in some marine samples (Endo et al, 2020). To examine the biogeography of the Asfarvirus MAGs in more detail we conducted a fragment recruitment analysis using reads from the Tara oceans expedition (Sunagawa et al, 2015).…”

Section: Resultsmentioning

confidence: 99%

“…Some families of NCLDV such as the Poxviridae, Asfarviridae, Iridoviridae , and Phycodnaviridae have been studied for decades, while others, such as the Pandoraviridae, Mimiviridae, and Marseilleviridae, have been discovered relatively recently (Raoult et al, 2004; Boyer et al, 2009; Philippe et al, 2013; Abergel et al, 2015). Although amoebae have been used as an effective system to cultivate many recently-discovered NCLDV, recent cultivation-independent studies have discovered a wide range of these viruses in diverse environments, suggesting that uncultivated members of this viral phylum are ubiquitous in the biosphere (Monier et al, 2008; Hingamp et al, 2013; Bäckström et al, 2019; Endo et al, 2020; Moniruzzaman et al, 2020a; Schulz et al, 2020). Given the notable complexity of NCLDVs and their cosmopolitan distribution, there is a need to better understand their genomic diversity and biogeography.…”

Section: Introductionmentioning

confidence: 99%

Comparative Genomics and Environmental Distribution of Large dsDNA viruses in the familyAsfarviridae

Karki

Moniruzzaman

Aylward

2021

Preprint

View full text Add to dashboard Cite

The Asfarviridae is a family of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) of which African swine fever virus (ASFV) is the most well-characterized. Recently the discovery of several Asfarviridae members other than ASFV has suggested that this family represents a diverse and cosmopolitan group of viruses, but the genomics and distribution of this family have not been studied in detail. To this end we analyzed five complete genomes and 35 metagenome-assembled genomes (MAGs) of viruses from this family to shed light on their evolutionary relationships and environmental distribution. The Asfarvirus MAGs derive from diverse marine, freshwater, and terrestrial habitats, underscoring the broad environmental distribution of this family. We present phylogenetic analyses using conserved marker genes and whole-genome comparison of pairwise average amino acid identity values, revealing a high level of genomic divergence across disparate Asfarviruses. Further, we found that Asfarviridae genomes encode genes with diverse predicted metabolic roles and detectable sequence homology to proteins in bacteria, archaea, and different eukaryotes, highlighting the genomic chimerism that is a salient feature of NCLDV. Our read mapping from Tara oceans metagenomic data also revealed that three Asfarviridae MAGs were present in multiple marine samples, indicating that they are widespread in the ocean. In one of these MAGs we identified four marker genes with >95% amino acid identity to genes sequenced from a virus that infects the dinoflagellate Heterocapsa circularisquama (HcDNAV). This suggests a potential host for this MAG, which would thereby represent a near-complete genome of a dinoflagellate-infecting giant virus. Together, these results show that Asfarviridae are ubiquitous, comprise similar sequence divergence as other NCLDV families, and include several members that are widespread in the ocean and potentially infect ecologically important protists.

show abstract

“…The family Mimiviridae is a major group of large DNA viruses that infect diverse eukaryotes in marine environments (31). A recent study revealed an association between eukaryote communities and Mimiviridae in a global metagenomic dataset (32). Another study detected cooccurring pairs of eukaryotes and large DNA viruses including members of the Mimiviridae through time-series sampling for more than 1 year in Northern Skagerrak, South Norway (18).…”

Section: Introductionmentioning

confidence: 99%

Year-round dynamics of amplicon sequence variant communities differ among eukaryotes,Mimiviridae, and prokaryotes in a coastal ecosystem

Prodinger

Endo

Takano

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Coastal seawater is the habitat of diverse microbial communities. These communities are affected by seasonal environmental changes and fluctuating nutrient availability, as well as competitive and cooperative interspecific interactions. The complex interplay of these factors affects elemental cycles and therefore, the environment, which in turn affects microbial communities. In this work, we investigated the seasonal dynamics of communities of eukaryotes, a major group of double-stranded DNA viruses infecting eukaryotes (i.e., Mimiviridae), as well as prokaryotes in the Uranouchi Inlet, Kochi, Japan. This inlet harbors several microalgae that recurrently form blooms throughout the year. We performed metabarcoding using ribosomal RNA genes and a Mimiviridae DNA polymerase gene as marker genes and counted cells of major algal species in 43 seawater samples collected during 20 months. Communities of eukaryotes, Mimiviridae, and prokaryotes characterized at the amplicon sequence variant (ASV) level showed similar seasonal cycles but differences in several aspects such as the recovery rate after a year. The ASV persistence level differed among eukaryote, Mimiviridae, and prokaryote communities. Mimiviridae ASVs were less persistent than were eukaryotic ASVs, and prokaryotic ASVs were the most persistent. These observations are discussed in the context of survival strategies of the major microbes in these three communities.

show abstract

Biogeography of marine giant viruses reveals their interplay with eukaryotes and ecological functions

Cited by 103 publications

References 73 publications

Quantitative assessment of NCLDV–host interactions predicted by co-occurrence analyses

Quantitative assessment of NCLDV–host interactions predicted by co-occurrence analyses

Comparative Genomics and Environmental Distribution of Large dsDNA viruses in the familyAsfarviridae

Year-round dynamics of amplicon sequence variant communities differ among eukaryotes,Mimiviridae, and prokaryotes in a coastal ecosystem

Contact Info

Product

Resources

About