scholarly journals Molecular fossils reveal ancient associations of dsDNA viruses with several phyla of fungi

2020 ◽  
Vol 6 (1) ◽  
Author(s):  
Zhen Gong ◽  
Yu Zhang ◽  
Guan-Zhu Han

Abstract Little is known about the infections of double-stranded DNA (dsDNA) viruses in fungi. Here, we use a paleovirological method to systematically identify the footprints of past dsDNA virus infections within the fungal genomes. We uncover two distinct groups of endogenous nucleocytoplasmic large DNA viruses (NCLDVs) in at least seven fungal phyla (accounting for about a third of known fungal phyla), revealing an unprecedented diversity of dsDNA viruses in fungi. Interestingly, one fungal dsDNA virus lineage infecting six fungal phyla is closely related to the giant virus Pithovirus, suggesting giant virus relatives might widely infect fungi. Co-speciation analyses indicate fungal NCLDVs mainly evolved through cross-species transmission. Taken together, our findings provide novel insights into the diversity and evolution of NCLDVs in fungi.

2016 ◽  
Vol 12 (3) ◽  
pp. 20160023 ◽  
Author(s):  
Rachel L. Nifong ◽  
James F. Gillooly

Heterogeneity in rates of survival, growth and reproduction among viruses is related to virus particle (i.e. virion) size, but we have little understanding of the factors that govern the four to five orders of magnitude in virus size variation. Here, we analyse variation in virion size in 67 double-stranded DNA viruses (i.e. dsDNA) that span all major biomes, and infect organisms ranging from single-celled prokaryotes to multicellular eukaryotes. We find that two metrics of virion size (i.e. virion volume and genome length) decrease by about 55-fold as the temperature of occurrence increases from 0 to 40°C. We also find that gene overlap increases exponentially with temperature, such that smaller viruses have proportionally greater gene overlap at higher temperatures. These results indicate dsDNA virus size increases with environmental temperature in much the same way as the cell or genome size of many host species.


2020 ◽  
Author(s):  
Gabriel J Starrett ◽  
Michael J Tisza ◽  
Nicole L Welch ◽  
Anna K Belford ◽  
Alberto Peretti ◽  
...  

Abstract Polintons (also known as Mavericks) were initially identified as a widespread class of eukaryotic transposons named for their hallmark type B DNA polymerase and retrovirus-like integrase genes. It has since been recognized that many polintons encode possible capsid proteins and viral genome-packaging ATPases similar to those of a diverse range of double-stranded DNA (dsDNA) viruses. This supports the inference that at least some polintons are actually viruses capable of cell-to-cell spread. At present, there are no polinton-associated capsid protein genes annotated in public sequence databases. To rectify this deficiency, we used a data-mining approach to investigate the distribution and gene content of polinton-like elements and related DNA viruses in animal genomic and metagenomic sequence datasets. The results define a discrete family-like clade of viruses with two genus-level divisions. We propose the family name Adintoviridae, connoting similarities to adenovirus virion proteins and the presence of a retrovirus-like integrase gene. Although adintovirus-class PolB sequences were detected in datasets for fungi and various unicellular eukaryotes, sequences resembling adintovirus virion proteins and accessory genes appear to be restricted to animals. Degraded adintovirus sequences are endogenized into the germlines of a wide range of animals, including humans.


2019 ◽  
Vol 116 (39) ◽  
pp. 19585-19592 ◽  
Author(s):  
Julien Guglielmini ◽  
Anthony C. Woo ◽  
Mart Krupovic ◽  
Patrick Forterre ◽  
Morgan Gaia

Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.


2015 ◽  
Vol 112 (38) ◽  
pp. E5318-E5326 ◽  
Author(s):  
Guillaume Blanc ◽  
Lucie Gallot-Lavallée ◽  
Florian Maumus

Virophages are recently discovered double-stranded DNA virus satellites that prey on giant viruses (nucleocytoplasmic large DNA viruses; NCLDVs), which are themselves parasites of unicellular eukaryotes. This coupled parasitism can result in the indirect control of eukaryotic cell mortality by virophages. However, the details of such tripartite relationships remain largely unexplored. We have discovered ∼300 predicted genes of putative virophage origin in the nuclear genome of the unicellular alga Bigelowiella natans. Physical clustering of these genes indicates that virophage genomes are integrated into the B. natans genome. Virophage inserts show high levels of similarity and synteny between each other, indicating that they are closely related. Virophage genes are transcribed not only in the sequenced B. natans strain but also in other Bigelowiella isolates, suggesting that transcriptionally active virophage inserts are widespread in Bigelowiella populations. Evidence that B. natans is also a host to NCLDV members is provided by the identification of NCLDV inserts in its genome. These putative large DNA viruses may be infected by B. natans virophages. We also identify four repeated elements sharing structural and genetic similarities with transpovirons—a class of mobile elements first discovered in giant viruses—that were probably independently inserted in the B. natans genome. We argue that endogenized provirophages may be beneficial to both the virophage and B. natans by (i) increasing the chances for the virophage to coinfect the host cell with an NCLDV prey and (ii) defending the host cell against fatal NCLDV infections.


2021 ◽  
Author(s):  
Percy Mutseka Lunga ◽  
Oliver K.I Bezuidt ◽  
Miho Hirai ◽  
Yoshihiro Takaki ◽  
Taichi Yokokawa ◽  
...  

Abstract BackgroundDue to their role as obligate parasites of marine microorganisms, viruses are primary mediators of marine biogeochemical cycles. Recent studies have provided irrevocable evidence showing that viruses augment the metabolisms of bacteria and archaea through expression of auxiliary metabolic genes (AMGs). Several studies have shown that AMGs affect the biogeochemical recycling of sulphur and nitrogen but comparatively less is known regarding their influence on phosphorus recycling.ResultsHere, we provide the first insights regarding the potential effects of phosphorus limitation and AMGs on putative prokaryotic hosts in the euphotic zone of the South Atlantic Ocean (SAO). We identified 7,176 viral contigs that were clustered into 5,999 viral operational taxonomic units (vOTUs, >5kb). These SAO viral communities appear to be unique, as over 89% had no taxonomic assignment, possibly due to the genetic endemism in this ocean. Three phosphatases, phoN, gmhB and rnhA-cobC, were identified as P-cycle AMGs in both prokaryotic double-stranded DNA viruses and eukaryotic Nucleocytoplasmic Large DNA viruses. These genes are associated with the acquisition of inorganic phosphate from phosphate esters, the largest reservoir of P-containing compounds in the marine environment. AMGs were identified in both uncultured and unclassified prokaryotic double-stranded DNA viruses predicted to infect Bacteriodetes, Proteobacteria, Chloroflexota and Poseidonales lineages. ConclusionTogether, these results suggest that viruses modulate P-cycling in euphotic zones of the ocean and that the acquisition of these phosphatase genes may be cues of P-ester stress.


2021 ◽  
Author(s):  
Grace Kago ◽  
Susan Parrish

AbstractThe giant Mimivirus is a member of the nucleocytoplasmic large DNA viruses (NCLDV), a group of diverse viruses that contain double-stranded DNA (dsDNA) genomes that replicate primarily in eukaryotic hosts. Two members of the NCLDV, Vaccinia Virus (VACV) and African Swine Fever Virus (ASFV), both synthesize Nudix enzymes that have been shown to decap mRNA, a process thought to accelerate viral and host mRNA turnover and promote the shutoff of host protein synthesis. Mimivirus encodes two Nudix enzymes in its genome, denoted as L375 and L534. Importantly, L375 exhibits sequence similarity to ASFV-DP and eukaryotic Dcp2, two Nudix enzymes shown to possess mRNA decapping activity. In this work, we demonstrate that recombinant Mimivirus L375 cleaves the 5’ m7GpppN mRNA cap, releasing m7GDP as a product. L375 did not significantly cleave mRNAs containing an unmethylated 5’GpppN cap, indicating that this enzyme specifically hydrolyzes methylated-capped transcripts. A point mutation in the L375 Nudix motif completely eliminated cap hydrolysis, showing that decapping activity is dependent on this motif. Addition of methylated cap derivatives or uncapped RNA inhibited L375 decapping activity, suggesting that L375 recognizes its substrate through interaction with both the mRNA cap and RNA body.


PLoS ONE ◽  
2021 ◽  
Vol 16 (9) ◽  
pp. e0245820
Author(s):  
Grace Kago ◽  
Susan Parrish

The giant Mimivirus is a member of the nucleocytoplasmic large DNA viruses (NCLDV), a group of diverse viruses that contain double-stranded DNA (dsDNA) genomes that replicate primarily in eukaryotic hosts. Two members of the NCLDV, Vaccinia Virus (VACV) and African Swine Fever Virus (ASFV), both synthesize Nudix enzymes that have been shown to decap mRNA, a process thought to accelerate viral and host mRNA turnover and promote the shutoff of host protein synthesis. Mimivirus encodes two Nudix enzymes in its genome, denoted as L375 and L534. Importantly, L375 exhibits sequence similarity to ASFV-DP and eukaryotic Dcp2, two Nudix enzymes shown to possess mRNA decapping activity. In this work, we demonstrate that recombinant Mimivirus L375 cleaves the 5’ m7GpppN mRNA cap, releasing m7GDP as a product. L375 did not significantly cleave mRNAs containing an unmethylated 5’GpppN cap, indicating that this enzyme specifically hydrolyzes methylated-capped transcripts. A point mutation in the L375 Nudix motif completely eliminated cap hydrolysis, showing that decapping activity is dependent on this motif. Addition of uncapped RNA significantly reduced L375 decapping activity, suggesting that L375 may recognize its substrate through interaction with the RNA body.


2018 ◽  
Author(s):  
Julien Guglielmini ◽  
Anthony Woo ◽  
Mart Krupovic ◽  
Patrick Forterre ◽  
Morgan Gaia

AbstractGiant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution and potential roles in the emergence of modern eukaryotes remain a subject of intense debate. Since the characterization of the mimivirus in 2003, many big and giant viruses have been discovered at a steady pace, offering a vast material for evolutionary investigations. In parallel, phylogenetic tools are constantly being improved, offering more rigorous approaches for reconstruction of deep evolutionary history of viruses and their hosts. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of two superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were seemingly transferred from two clades of NCLDVs to proto-eukaryotes, giving rise to two of the three eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.


2021 ◽  
Vol 1 (1) ◽  
Author(s):  
Benjamin Bolduc ◽  
Olivier Zablocki ◽  
Jiarong Guo ◽  
Ahmed A. Zayed ◽  
Dean Vik ◽  
...  

AbstractMicrobes drive myriad ecosystem processes, but under strong influence from viruses. Because studying viruses in complex systems requires different tools than those for microbes, they remain underexplored. To combat this, we previously aggregated double-stranded DNA (dsDNA) virus analysis capabilities and resources into ‘iVirus’ on the CyVerse collaborative cyberinfrastructure. Here we substantially expand iVirus’s functionality and accessibility, to iVirus 2.0, as follows. First, core iVirus apps were integrated into the Department of Energy’s Systems Biology KnowledgeBase (KBase) to provide an additional analytical platform. Second, at CyVerse, 20 software tools (apps) were upgraded or added as new tools and capabilities. Third, nearly 20-fold more sequence reads were aggregated to capture new data and environments. Finally, documentation, as “live” protocols, was updated to maximize user interaction with and contribution to infrastructure development. Together, iVirus 2.0 serves as a uniquely central and accessible analytical platform for studying how viruses, particularly dsDNA viruses, impact diverse microbial ecosystems.


mSystems ◽  
2020 ◽  
Vol 5 (3) ◽  
Author(s):  
Frederik Schulz ◽  
Julien Andreani ◽  
Rania Francis ◽  
Hadjer Boudjemaa ◽  
Jacques Yaacoub Bou Khalil ◽  
...  

ABSTRACT Giant viruses have large genomes, often within the size range of cellular organisms. This distinguishes them from most other viruses and demands additional effort for the successful recovery of their genomes from environmental sequence data. Here, we tested the performance of genome-resolved metagenomics on a recently isolated giant virus, Fadolivirus, by spiking it into an environmental sample from which two other giant viruses were isolated. At high spike-in levels, metagenome assembly and binning led to the successful genomic recovery of Fadolivirus from the sample. A complementary survey of the major capsid protein indicated the presence of other giant viruses in the sample matrix but did not detect the two isolated from this sample. Our results indicate that genome-resolved metagenomics is a valid approach for the recovery of near-complete giant virus genomes given that sufficient clonal particles are present. However, our data also underline that a vast majority of giant viruses remain currently undetected, even in an era of terabase-scale metagenomics. IMPORTANCE The discovery of large and giant nucleocytoplasmic large DNA viruses (NCLDV) with genomes in the megabase range and equipped with a wide variety of features typically associated with cellular organisms was one of the most unexpected, intriguing, and spectacular breakthroughs in virology. Recent studies suggest that these viruses are highly abundant in the oceans, freshwater, and soil, impact the biology and ecology of their eukaryotic hosts, and ultimately affect global nutrient cycles. Genome-resolved metagenomics is becoming an increasingly popular tool to assess the diversity and coding potential of giant viruses, but this approach is currently lacking validation.


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