scholarly journals A phylogenomic framework for charting the diversity and evolution of giant viruses

PLoS Biology ◽  
2021 ◽  
Vol 19 (10) ◽  
pp. e3001430
Author(s):  
Frank O. Aylward ◽  
Mohammad Moniruzzaman ◽  
Anh D. Ha ◽  
Eugene V. Koonin
Keyword(s):  
Giant Virus ◽  
Phylogenomic Analysis ◽  
Environmental Distribution ◽  
Dna Viruses ◽  
Giant Viruses ◽  
Taxonomic Framework

Large DNA viruses of the phylum Nucleocytoviricota have recently emerged as important members of ecosystems around the globe that challenge traditional views of viral complexity. Numerous members of this phylum that cannot be classified within established families have recently been reported, and there is presently a strong need for a robust phylogenomic and taxonomic framework for these viruses. Here, we report a comprehensive phylogenomic analysis of the Nucleocytoviricota, present a set of giant virus orthologous groups (GVOGs) together with a benchmarked reference phylogeny, and delineate a hierarchical taxonomy within this phylum. We show that the majority of Nucleocytoviricota diversity can be partitioned into 6 orders, 32 families, and 344 genera, substantially expanding the number of currently recognized taxonomic ranks for these viruses. We integrate our results within a taxonomy that has been adopted for all viruses to establish a unifying framework for the study of Nucleocytoviricota diversity, evolution, and environmental distribution.

scholarly journals Virus Genomes from Deep Sea Sediments Expand the Ocean Megavirome and Support Independent Origins of Viral Gigantism

mBio ◽  
2019 ◽  
Vol 10 (2) ◽  
Author(s):  
Disa Bäckström ◽  
Natalya Yutin ◽  
Steffen L. Jørgensen ◽  
Jennah Dharamshi ◽  
Felix Homa ◽  
...  
Keyword(s):  
Deep Sea ◽  
Genomic Diversity ◽  
Genome Comparison ◽  
Phylogenomic Analysis ◽  
Dna Viruses ◽  
Deep Sea Sediments ◽  
Giant Viruses ◽  
Nucleocytoplasmic Large Dna Viruses ◽  
Loki’S Castle ◽  
Virus Genomes

ABSTRACT The nucleocytoplasmic large DNA viruses (NCLDV) of eukaryotes (proposed order, “Megavirales”) include the families Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, Phycodnaviridae, Marseilleviridae, and Mimiviridae, as well as still unclassified pithoviruses, pandoraviruses, molliviruses, and faustoviruses. Several of these virus groups include giant viruses, with genome and particle sizes exceeding those of many bacterial and archaeal cells. We explored the diversity of the NCLDV in deep sea sediments from the Loki’s Castle hydrothermal vent area. Using metagenomics, we reconstructed 23 high-quality genomic bins of novel NCLDV, 15 of which are related to pithoviruses, 5 to marseilleviruses, 1 to iridoviruses, and 2 to klosneuviruses. Some of the identified pithovirus-like and marseillevirus-like genomes belong to deep branches in the phylogenetic tree of core NCLDV genes, substantially expanding the diversity and phylogenetic depth of the respective groups. The discovered viruses, including putative giant members of the family Marseilleviridae, have a broad range of apparent genome sizes, in agreement with the multiple, independent origins of gigantism in different branches of the NCLDV. Phylogenomic analysis reaffirms the monophyly of the pithovirus-iridovirus-marseillevirus branch of the NCLDV. Similarly to other giant viruses, the pithovirus-like viruses from Loki’s Castle encode translation systems components. Phylogenetic analysis of these genes indicates a greater bacterial contribution than had been detected previously. Genome comparison suggests extensive gene exchange between members of the pithovirus-like viruses and Mimiviridae. Further exploration of the genomic diversity of Megavirales in additional sediment samples is expected to yield new insights into the evolution of giant viruses and the composition of the ocean megavirome. IMPORTANCE Genomics and evolution of giant viruses are two of the most vigorously developing areas of virus research. Lately, metagenomics has become the main source of new virus genomes. Here we describe a metagenomic analysis of the genomes of large and giant viruses from deep sea sediments. The assembled new virus genomes substantially expand the known diversity of the nucleocytoplasmic large DNA viruses of eukaryotes. The results support the concept of independent evolution of giant viruses from smaller ancestors in different virus branches.

scholarly journals First evidence of host range expansion in virophages and its potential impact on giant viruses and host cells

2019 ◽  
Author(s):  
Said Mougari ◽  
Nisrine Chelkha ◽  
Dehia Sahmi-Bounsiar ◽  
Fabrizio Di Pinto ◽  
Philippe Colson ◽  
...  
Keyword(s):  
Host Range ◽  
Range Expansion ◽  
Virus Production ◽  
Host Cells ◽  
Giant Virus ◽  
Dna Viruses ◽  
Host Range Expansion ◽  
Parasitic Lifestyle ◽  
Giant Viruses ◽  
Viral Host Range

AbstractVirophages are satellite-like double stranded DNA viruses whose replication requires the presence of two biological entities, a giant virus and a protist. In this report, we present the first evidence of host range expansion in a virophage. We demonstrated that the Guarani virophage was able to spontaneously expand its viral host range to replicate with two novel giant viruses that were previously nonpermissive to this virophage. We were able to characterize a potential genetic determinant of this cross-species infection. We then highlighted the relevant impact of this host adaptation on giant viruses and protists by demonstrating that coinfection with the mutant virophage abolishes giant virus production and rescues the host cell population from lysis. The results of our study help to elucidate the parasitic lifestyle of virophages and their interactions with giant viruses and protists.

scholarly journals The Roles of Electrostatic Interactions in Capsid Assembly Mechanisms of Giant Viruses

2019 ◽  
Vol 20 (8) ◽  
pp. 1876 ◽  
Author(s):  
Yuejiao Xian ◽  
Chitra B. Karki ◽  
Sebastian Miki Silva ◽  
Lin Li ◽  
Chuan Xiao
Keyword(s):  
Self Assembly ◽  
Electrostatic Interactions ◽  
Virus Assembly ◽  
Binding Mode ◽  
Giant Virus ◽  
Capsid Assembly ◽  
Fold Axis ◽  
Binding Modes ◽  
Dna Viruses ◽  
Giant Viruses

In the last three decades, many giant DNA viruses have been discovered. Giant viruses present a unique and essential research frontier for studies of self-assembly and regulation of supramolecular assemblies. The question on how these giant DNA viruses assemble thousands of proteins so accurately to form their protein shells, the capsids, remains largely unanswered. Revealing the mechanisms of giant virus assembly will help to discover the mysteries of many self-assembly biology problems. Paramecium bursaria Chlorella virus-1 (PBCV-1) is one of the most intensively studied giant viruses. Here, we implemented a multi-scale approach to investigate the interactions among PBCV-1 capsid building units called capsomers. Three binding modes with different strengths are found between capsomers around the relatively flat area of the virion surface at the icosahedral 2-fold axis. Furthermore, a capsomer structure manipulation package is developed to simulate the capsid assembly process. Using these tools, binding forces among capsomers were investigated and binding funnels were observed that were consistent with the final assembled capsid. In addition, total binding free energies of each binding mode were calculated. The results helped to explain previous experimental observations. Results and tools generated in this work established an initial computational approach to answer current unresolved questions regarding giant virus assembly mechanisms. Results will pave the way for studying more complicated process in other biomolecular structures.

scholarly journals Advantages and Limits of Metagenomic Assembly and Binning of a Giant Virus

mSystems ◽  
2020 ◽  
Vol 5 (3) ◽  
Author(s):  
Frederik Schulz ◽  
Julien Andreani ◽  
Rania Francis ◽  
Hadjer Boudjemaa ◽  
Jacques Yaacoub Bou Khalil ◽  
...  
Keyword(s):  
Sequence Data ◽  
Giant Virus ◽  
Dna Viruses ◽  
Successful Recovery ◽  
Metagenome Assembly ◽  
Giant Viruses ◽  
Nucleocytoplasmic Large Dna Viruses ◽  
Metagenomic Assembly ◽  
Virus Genomes ◽  
Coding Potential

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.

scholarly journals In-depth study of Mollivirus sibericum, a new 30,000-y-old giant virus infecting Acanthamoeba

2015 ◽  
Vol 112 (38) ◽  
pp. E5327-E5335 ◽  
Author(s):  
Matthieu Legendre ◽  
Audrey Lartigue ◽  
Lionel Bertaux ◽  
Sandra Jeudy ◽  
Julia Bartoli ◽  
...  
Keyword(s):  
Global Warming ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Ribosomal Proteins ◽  
Acanthamoeba Castellanii ◽  
Giant Virus ◽  
Metagenomic Analysis ◽  
Dna Viruses ◽  
Depth Study ◽  
Giant Viruses

Acanthamoeba species are infected by the largest known DNA viruses. These include icosahedral Mimiviruses, amphora-shaped Pandoraviruses, and Pithovirus sibericum, the latter one isolated from 30,000-y-old permafrost. Mollivirus sibericum, a fourth type of giant virus, was isolated from the same permafrost sample. Its approximately spherical virion (0.6-µm diameter) encloses a 651-kb GC-rich genome encoding 523 proteins of which 64% are ORFans; 16% have their closest homolog in Pandoraviruses and 10% in Acanthamoeba castellanii probably through horizontal gene transfer. The Mollivirus nucleocytoplasmic replication cycle was analyzed using a combination of “omic” approaches that revealed how the virus highjacks its host machinery to actively replicate. Surprisingly, the host’s ribosomal proteins are packaged in the virion. Metagenomic analysis of the permafrost sample uncovered the presence of both viruses, yet in very low amount. The fact that two different viruses retain their infectivity in prehistorical permafrost layers should be of concern in a context of global warming. Giant viruses’ diversity remains to be fully explored.

scholarly journals Virus genomes from deep sea sediments expand the ocean megavirome and support independent origins of viral gigantism

2018 ◽  
Author(s):  
Disa Bäckström ◽  
Natalya Yutin ◽  
Steffen L. Jørgensen ◽  
Jennah Dharamshi ◽  
Felix Homa ◽  
...  
Keyword(s):  
Deep Sea ◽  
Genomic Diversity ◽  
Genome Comparison ◽  
Phylogenomic Analysis ◽  
Dna Viruses ◽  
Deep Sea Sediments ◽  
Giant Viruses ◽  
Nucleocytoplasmic Large Dna Viruses ◽  
Loki’S Castle ◽  
Virus Genomes

AbstractThe Nucleocytoplasmic Large DNA Viruses (NCLDV) of eukaryotes (proposed order ”Megavirales”) include the families Poxviridae, Asfarviridae, Iridoviridae, Ascoviridae, Phycodnaviridae, Marseilleviridae, and Mimiviridae, as well as still unclassified Pithoviruses, Pandoraviruses, Molliviruses and Faustoviruses. Several of these virus groups include giant viruses, with genome and particle sizes exceeding those of many bacterial and archaeal cells. We explored the diversity of the NCLDV in deep-sea sediments from the Loki’s Castle hydrothermal vent area. Using metagenomics, we reconstructed 23 high quality genomic bins of novel NCLDV, 15 of which are closest related to Pithoviruses, 5 to Marseilleviruses, 1 to Iridoviruses, and 2 to Klosneuviruses. Some of the identified Pitho-like and Marseille-like genomes belong to deep branches in the phylogenetic tree of core NCLDV genes, substantially expanding the diversity and phylogenetic depth of the respective groups. The discovered viruses have a broad range of apparent genome sizes including putative giant members of the family Marseilleviridae, in agreement with multiple, independent origins of gigantism in different branches of the NCLDV. Phylogenomic analysis reaffirms the monophyly of the Pitho-Irido-Marseille branch of NCLDV. Similarly to other giant viruses, the Pitho-like viruses from Loki’s Castle encode translation systems components. Phylogenetic analysis of these genes indicates a greater bacterial contribution than detected previously. Genome comparison suggests extensive gene exchange between members of the Pitho-like viruses and Mimiviridae. Further exploration of the genomic diversity of “Megavirales” in additional sediment samples is expected to yield new insights into the evolution of giant viruses and the composition of the ocean megavirome.ImportanceGenomics and evolution of giant viruses is one of the most vigorously developing areas of virus research. Lately, metagenomics has become the main source of new virus genomes. Here we describe a metagenomic analysis of the genomes of large and giant viruses from deep sea sediments. The assembled new virus genomes substantially expand the known diveristy of the Nucleo-Cytoplasmic Large DNA Viruses of eukaryotes. The results support the concept of independent evolution of giant viruses from smaller ancestors in different virus branches.

scholarly journals Giant Viruses and the Tree of Life

2021 ◽  
Vol 6 (2) ◽  
Author(s):  
Patrick Forterre
Keyword(s):  
Tree Of Life ◽  
Current Understanding ◽  
Giant Virus ◽  
Giant Viruses

When the first giant virus, the mimivirus, was discovered in 1992, it was misidentified as a bacterium because it was too large to have been a virus by the current understanding. Ever since, biologists have been debating how viruses should be categorized and described. Are they living? Are they something else? What is their place on the tree of life?

scholarly journals Advantages and limits of metagenomic assembly and binning of a giant virus

2020 ◽  
Author(s):  
Frederik Schulz ◽  
Julien Andreani ◽  
Rania Francis ◽  
Jacques Yaacoub Bou Khalil ◽  
Janey Lee ◽  
...  
Keyword(s):  
Size Range ◽  
Sequence Data ◽  
Giant Virus ◽  
Sample Matrix ◽  
Environmental Sequence ◽  
Successful Recovery ◽  
Metagenome Assembly ◽  
Giant Viruses ◽  
Metagenomic Assembly ◽  
Virus Genomes

AbstractGiant 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 viral hallmark genes 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. Our data also underline that a vast majority of giant viruses remain currently undetected, even in an era of terabase-scale metagenomics.

scholarly journals Boiling Acid Mimics Intracellular Giant Virus Genome Release

2019 ◽  
Author(s):  
Jason R. Schrad ◽  
Jônatas S. Abrahão ◽  
Juliana R. Cortines ◽  
Kristin N. Parent
Keyword(s):  
Mass Spectrometry ◽  
Virus Infection ◽  
Virus Genome ◽  
Life Cycles ◽  
Giant Virus ◽  
Infection Mechanisms ◽  
Specific Proteins ◽  
Giant Viruses ◽  
Molecular Forces

SummarySince their discovery, giant viruses have expanded our understanding of the principles of virology. Due to their gargantuan size and complexity, little is known about the life cycles of these viruses. To answer outstanding questions regarding giant virus infection mechanisms, we set out to determine biomolecular conditions that promote giant virus genome release. We generated four metastable infection intermediates in Samba virus (lineage A Mimiviridae) as visualized by cryo-EM, cryo-ET, and SEM. Each of these four intermediates reflects a stage that occurs in vivo. We show that these genome release stages are conserved in other, diverse giant viruses. Finally, we identified proteins that are released from Samba and newly discovered Tupanvirus through differential mass spectrometry. Our work revealed the molecular forces that trigger infection are conserved amongst disparate giant viruses. This study is also the first to identify specific proteins released during the initial stages of giant virus infection.

scholarly journals Giant virus vs amoeba: fight for supremacy

2019 ◽  
Vol 16 (1) ◽  
Author(s):  
Graziele Oliveira ◽  
Bernard La Scola ◽  
Jônatas Abrahão
Keyword(s):  
Giant Virus ◽  
Host Pathogen Interactions ◽  
Free Living ◽  
Host Interactions ◽  
Virus Particles ◽  
Recent Advances ◽  
Host Pathogen ◽  
New Hosts ◽  
Giant Viruses

Abstract Since the discovery of mimivirus, numerous giant viruses associated with free-living amoebae have been described. The genome of giant viruses can be more than 2.5 megabases, and virus particles can exceed the size of many bacteria. The unexpected characteristics of these viruses have made them intriguing research targets and, as a result, studies focusing on their interactions with their amoeba host have gained increased attention. Studies have shown that giant viruses can establish host–pathogen interactions, which have not been previously demonstrated, including the unprecedented interaction with a new group of small viruses, called virophages, that parasitize their viral factories. In this brief review, we present recent advances in virophage–giant virus–host interactions and highlight selected studies involving interactions between giant viruses and amoebae. These unprecedented interactions involve the giant viruses mimivirus, marseillevirus, tupanviruses and faustovirus, all of which modulate the amoeba environment, affecting both their replication and their spread to new hosts.

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