The Experts below are selected from a list of 270 Experts worldwide ranked by ideXlab platform
Bernard La Scola - One of the best experts on this subject based on the ideXlab platform.
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a Virophage cross species infection through mutant selection represses giant virus propagation promoting host cell survival
Communications Biology, 2020Co-Authors: Said Mougari, Philippe Colson, Nisrine Chelkha, Fabrizio Di Pinto, Jonatas Santos Abrahao, Dehia Sahmibounsiar, Bernard La ScolaAbstract:Virus adaptation to new hosts is a major cause of infectious disease emergence. This mechanism has been intensively studied in the context of zoonotic virus spillover, due to its impact on global health. However, it remains unclear for Virophages, parasites of giant viruses and potential regulators of microbial communities. Here, we present, for the first time to our knowledge, evidence of cross-species infection of a Virophage. We demonstrated that challenging the native population of Guarani Virophage with two previously unidentified giant viruses, previously nonpermissive to this Virophage, allows the selection of a mutant genotype able to infect these giant viruses. We were able to characterize the potential genetic determinant (deletion) carried by the Virophage with the expanded-host range. Our study also highlights the relevant biological impact of this host adaptation by demonstrating that coinfection with the mixture containing the mutant Virophage abolishes giant virus production and rescues the host cell population from lysis.
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A Virophage cross-species infection through mutant selection represses giant virus propagation, promoting host cell survival
Communications Biology, 2020Co-Authors: Said Mougari, Philippe Colson, Jonatas Abrahao, Nisrine Chelkha, Dehia Sahmi-bounsiar, Fabrizio Di Pinto, Bernard La ScolaAbstract:Virus adaptation to new hosts is a major cause of infectious disease emergence. This mechanism has been intensively studied in the context of zoonotic virus spillover, due to its impact on global health. However, it remains unclear for Virophages, parasites of giant viruses and potential regulators of microbial communities. Here, we present, for the first time to our knowledge, evidence of cross-species infection of a Virophage. We demonstrated that challenging the native population of Guarani Virophage with two previously unidentified giant viruses, previously nonpermissive to this Virophage, allows the selection of a mutant genotype able to infect these giant viruses. We were able to characterize the potential genetic determinant (deletion) carried by the Virophage with the expanded-host range. Our study also highlights the relevant biological impact of this host adaptation by demonstrating that coinfection with the mixture containing the mutant Virophage abolishes giant virus production and rescues the host cell population from lysis. Mougari et al. show that coinfection with a mixture containing mutant Virophages abolishes the production of their host giant viruses, protecting the cells infected with these giant viruses. This study provides insights into multi-level parasitic interactions among Virophages, giant viruses, and protists.
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guarani Virophage a new sputnik like isolate from a brazilian lake
Frontiers in Microbiology, 2019Co-Authors: Said Mougari, Meriem Bekliz, Anthony Levasseur, Fabrizio Di Pinto, Jonatas Santos Abrahao, Bernard La ScolaAbstract:Virophages are critical regulators of viral population dynamics and potential actors in the stability of the microbial networks. These small biological entities predate the replicative cycle of giant viruses, such as the members of the Mimiviridae family or their distant relatives, which produce within the cytoplasm of their host cells a viral factory harboring a complex biochemistry propitious to the growth of the smaller parasites. In this paper, we describe the isolation and the characterization of a new Virophage, the eighth, that we named Guarani. We observed that Guarani exhibits a late replication cycle compared to its giant virus host. In addition, like all Sputnik strains, Guarani is able to infect the three lineages A, B and C of the Mimiviridae family, and affects the replication and the infectivity of its host virus. In terms of genetic content, Guarani has a 18,967 bp long double-stranded DNA genome encoding 22 predicted genes very similar to Sputnik genes, except for ORF19 and ORF12. The former is more related to Zamilon while the latter seems to be novel. The architecture of the Guarani genome is closely related to Sputnik and Zamilon strains, suggesting a common origin for all these Virophages.
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Image_1_Role of the R349 Gene and Its Repeats in the MIMIVIRE Defense System.TIF
2019Co-Authors: Said Mougari, Jonatas Abrahao, Graziele P. Oliveira, Jacques Bou Y. Khalil, Bernard La ScolaAbstract:MIMIVIRE is a defense system described in lineage A Mimivirus (Mimiviridae family) that mediates resistance against Zamilon Virophage. It is composed of putative helicase and nuclease associated with a gene of unknown function called R349, which contains four 15 bp repeats homologous to the Virophage sequence. In a previous study, the silencing of such genes restored Virophage susceptibility. Moreover, the CRISPR Cas-4 like activity of the nuclease has recently been characterized. In this study, a recently isolated Mimivirus of lineage A with R349 gene lacking 3 of 4 repeats was demonstrated to be susceptible to Zamilon. To reinforce the importance of the R349 gene in the MIMIVIRE system, we developed and presented, for the first time to our knowledge, a protocol for Mimivirus genomic editing. By knocking out R349 gene in a Mimivirus lineage A, we observed the replication of Zamilon, indicating that this gene is critical in the resistance against this specific group of Virophages.
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Table_1_Role of the R349 Gene and Its Repeats in the MIMIVIRE Defense System.XLSX
2019Co-Authors: Said Mougari, Jonatas Abrahao, Graziele P. Oliveira, Jacques Bou Y. Khalil, Bernard La ScolaAbstract:MIMIVIRE is a defense system described in lineage A Mimivirus (Mimiviridae family) that mediates resistance against Zamilon Virophage. It is composed of putative helicase and nuclease associated with a gene of unknown function called R349, which contains four 15 bp repeats homologous to the Virophage sequence. In a previous study, the silencing of such genes restored Virophage susceptibility. Moreover, the CRISPR Cas-4 like activity of the nuclease has recently been characterized. In this study, a recently isolated Mimivirus of lineage A with R349 gene lacking 3 of 4 repeats was demonstrated to be susceptible to Zamilon. To reinforce the importance of the R349 gene in the MIMIVIRE system, we developed and presented, for the first time to our knowledge, a protocol for Mimivirus genomic editing. By knocking out R349 gene in a Mimivirus lineage A, we observed the replication of Zamilon, indicating that this gene is critical in the resistance against this specific group of Virophages.
Philippe Colson - One of the best experts on this subject based on the ideXlab platform.
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a Virophage cross species infection through mutant selection represses giant virus propagation promoting host cell survival
Communications Biology, 2020Co-Authors: Said Mougari, Philippe Colson, Nisrine Chelkha, Fabrizio Di Pinto, Jonatas Santos Abrahao, Dehia Sahmibounsiar, Bernard La ScolaAbstract:Virus adaptation to new hosts is a major cause of infectious disease emergence. This mechanism has been intensively studied in the context of zoonotic virus spillover, due to its impact on global health. However, it remains unclear for Virophages, parasites of giant viruses and potential regulators of microbial communities. Here, we present, for the first time to our knowledge, evidence of cross-species infection of a Virophage. We demonstrated that challenging the native population of Guarani Virophage with two previously unidentified giant viruses, previously nonpermissive to this Virophage, allows the selection of a mutant genotype able to infect these giant viruses. We were able to characterize the potential genetic determinant (deletion) carried by the Virophage with the expanded-host range. Our study also highlights the relevant biological impact of this host adaptation by demonstrating that coinfection with the mixture containing the mutant Virophage abolishes giant virus production and rescues the host cell population from lysis.
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A Virophage cross-species infection through mutant selection represses giant virus propagation, promoting host cell survival
Communications Biology, 2020Co-Authors: Said Mougari, Philippe Colson, Jonatas Abrahao, Nisrine Chelkha, Dehia Sahmi-bounsiar, Fabrizio Di Pinto, Bernard La ScolaAbstract:Virus adaptation to new hosts is a major cause of infectious disease emergence. This mechanism has been intensively studied in the context of zoonotic virus spillover, due to its impact on global health. However, it remains unclear for Virophages, parasites of giant viruses and potential regulators of microbial communities. Here, we present, for the first time to our knowledge, evidence of cross-species infection of a Virophage. We demonstrated that challenging the native population of Guarani Virophage with two previously unidentified giant viruses, previously nonpermissive to this Virophage, allows the selection of a mutant genotype able to infect these giant viruses. We were able to characterize the potential genetic determinant (deletion) carried by the Virophage with the expanded-host range. Our study also highlights the relevant biological impact of this host adaptation by demonstrating that coinfection with the mixture containing the mutant Virophage abolishes giant virus production and rescues the host cell population from lysis. Mougari et al. show that coinfection with a mixture containing mutant Virophages abolishes the production of their host giant viruses, protecting the cells infected with these giant viruses. This study provides insights into multi-level parasitic interactions among Virophages, giant viruses, and protists.
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giant viruses of amoebae a journey through innovative research and paradigm changes
Annual Review of Virology, 2017Co-Authors: Philippe Colson, Bernard La Scola, Didier RaoultAbstract:Giant viruses of amoebae were discovered serendipitously in 2003; they are visible via optical microscopy, making them bona fide microbes. Their lifestyle, structure, and genomes break the mold of classical viruses. Giant viruses of amoebae are complex microorganisms. Their genomes harbor between 444 and 2,544 genes, including many that are unique to viruses, and encode translation components; their virions contain >100 proteins as well as mRNAs. Mimiviruses have a specific mobilome, including Virophages, proVirophages, and transpovirons, and can resist Virophages through a system known as MIMIVIRE (mimivirus Virophage resistance element). Giant viruses of amoebae bring upheaval to the definition of viruses and tend to separate the current virosphere into two categories: very simple viruses and viruses with complexity similar to that of other microbes. This new paradigm is propitious for enhanced detection and characterization of giant viruses of amoebae, and a particular focus on their role in humans is ...
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mimivirus leading the way in the discovery of giant viruses of amoebae
Nature Reviews Microbiology, 2017Co-Authors: Philippe Colson, Bernard La Scola, Anthony Levasseur, Gustavo CaetanoanollesAbstract:The discovery of the giant amoebal virus mimivirus, in 2003, opened up a new area of virology. Extended studies, including those of mimiviruses, have since revealed that these viruses have genetic, proteomic and structural features that are more complex than those of conventional viruses. The accidental discovery of the giant virus of amoeba — Acanthamoeba polyphaga mimivirus (APMV; more commonly known as mimivirus) — in 2003 changed the field of virology. Viruses were previously defined by their submicroscopic size, which probably prevented the search for giant viruses, which are visible by light microscopy. Extended studies of giant viruses of amoebae revealed that they have genetic, proteomic and structural complexities that were not thought to exist among viruses and that are comparable to those of bacteria, archaea and small eukaryotes. The giant virus particles contain mRNA and more than 100 proteins, they have gene repertoires that are broader than those of other viruses and, notably, some encode translation components. The infection cycles of giant viruses of amoebae involve virus entry by amoebal phagocytosis and replication in viral factories. In addition, mimiviruses are infected by Virophages, defend against them through the mimivirus Virophage resistance element (MIMIVIRE) system and have a unique mobilome. Overall, giant viruses of amoebae, including mimiviruses, marseilleviruses, pandoraviruses, pithoviruses, faustoviruses and molliviruses, challenge the definition and classification of viruses, and have increasingly been detected in humans.
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giant viruses of amoebas an update
Frontiers in Microbiology, 2016Co-Authors: Sarah Aherfi, Philippe Colson, Bernard La ScolaAbstract:During the 12 past years, five new or putative virus families encompassing several members, namely Mimiviridae, Marseilleviridae, pandoraviruses, faustoviruses, and Virophages were described. In addition, Pithovirus sibericum and Mollivirus sibericum represent type strains of putative new giant virus families. All these viruses were isolated using amoebal coculture methods. These giant viruses were linked by phylogenomic analyses to other large DNA viruses. They were then proposed to be classified in a new viral order, the Megavirales, on the basis of their common origin, as shown by a set of ancestral genes encoding key viral functions, a common virion architecture, and shared major biological features including replication inside cytoplasmic factories. Megavirales is increasingly demonstrated to stand in the tree of life aside Bacteria, Archaea, and Eukarya, and the megavirus ancestor is suspected to be as ancient as cellular ancestors. In addition, giant amoebal viruses are visible under a light microscope and display many phenotypic and genomic features not found in other viruses, while they share other characteristics with parasitic microbes. Moreover, these organisms appear to be common inhabitants of our biosphere, and mimiviruses and marseilleviruses were isolated from human samples and associated to diseases. In the present review, we describe the main features and recent findings on these giant amoebal viruses and Virophages.
Eugene V. Koonin - One of the best experts on this subject based on the ideXlab platform.
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Genome and Environmental Activity of a Chrysochromulina parva Virus and Its Virophages
Frontiers Media S.A., 2019Co-Authors: Joshua M. A. Stough, Natalya Yutin, Eugene V. Koonin, Yuri V. Chaban, Mohammed Moniruzzaman, Eric R. Gann, Helena L. Pound, Morgan M. Steffen, Jenna N. Black, Steven W. WilhelmAbstract:Some giant viruses are ecological agents that are predicted to be involved in the top-down control of single-celled eukaryotic algae populations in aquatic ecosystems. Despite an increased interest in giant viruses since the discovery and characterization of Mimivirus and other viral giants, little is known about their physiology and ecology. In this study, we characterized the genome and functional potential of a giant virus that infects the freshwater haptophyte Chrysochromulina parva, originally isolated from Lake Ontario. This virus, CpV-BQ2, is a member of the nucleo-cytoplasmic large DNA virus (NCLDV) group and possesses a 437 kb genome encoding 503 ORFs with a GC content of 25%. Phylogenetic analyses of core NCLDV genes place CpV-BQ2 amongst the emerging group of algae-infecting Mimiviruses informally referred to as the “extended Mimiviridae,” making it the first virus of this group to be isolated from a freshwater ecosystem. During genome analyses, we also captured and described the genomes of three distinct Virophages that co-occurred with CpV-BQ2 and likely exploit CpV for their own replication. These Virophages belong to the polinton-like viruses (PLV) group and encompass 19–23 predicted genes, including all of the core PLV genes as well as several genes implicated in genome modifications. We used the CpV-BQ2 and Virophage reference sequences to recruit reads from available environmental metatranscriptomic data to estimate their activity in fresh waters. We observed moderate recruitment of both virus and Virophage transcripts in samples obtained during Microcystis aeruginosa blooms in Lake Erie and Lake Tai, China in 2013, with a spike in activity in one sample. Virophage transcript abundance for two of the three isolates strongly correlated with that of the CpV-BQ2. Together, the results highlight the importance of giant viruses in the environment and establish a foundation for future research on the physiology and ecology CpV-BQ2 as a model system for algal Mimivirus dynamics in freshwaters
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Data_Sheet_1_Genome and Environmental Activity of a Chrysochromulina parva Virus and Its Virophages.PDF
2019Co-Authors: Joshua M. A. Stough, Natalya Yutin, Eugene V. Koonin, Yuri V. Chaban, Mohammed Moniruzzaman, Eric R. Gann, Helena L. Pound, Morgan M. Steffen, Jenna N. Black, Steven W. WilhelmAbstract:Some giant viruses are ecological agents that are predicted to be involved in the top-down control of single-celled eukaryotic algae populations in aquatic ecosystems. Despite an increased interest in giant viruses since the discovery and characterization of Mimivirus and other viral giants, little is known about their physiology and ecology. In this study, we characterized the genome and functional potential of a giant virus that infects the freshwater haptophyte Chrysochromulina parva, originally isolated from Lake Ontario. This virus, CpV-BQ2, is a member of the nucleo-cytoplasmic large DNA virus (NCLDV) group and possesses a 437 kb genome encoding 503 ORFs with a GC content of 25%. Phylogenetic analyses of core NCLDV genes place CpV-BQ2 amongst the emerging group of algae-infecting Mimiviruses informally referred to as the “extended Mimiviridae,” making it the first virus of this group to be isolated from a freshwater ecosystem. During genome analyses, we also captured and described the genomes of three distinct Virophages that co-occurred with CpV-BQ2 and likely exploit CpV for their own replication. These Virophages belong to the polinton-like viruses (PLV) group and encompass 19–23 predicted genes, including all of the core PLV genes as well as several genes implicated in genome modifications. We used the CpV-BQ2 and Virophage reference sequences to recruit reads from available environmental metatranscriptomic data to estimate their activity in fresh waters. We observed moderate recruitment of both virus and Virophage transcripts in samples obtained during Microcystis aeruginosa blooms in Lake Erie and Lake Tai, China in 2013, with a spike in activity in one sample. Virophage transcript abundance for two of the three isolates strongly correlated with that of the CpV-BQ2. Together, the results highlight the importance of giant viruses in the environment and establish a foundation for future research on the physiology and ecology CpV-BQ2 as a model system for algal Mimivirus dynamics in freshwaters.
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ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue:DNA Habitats and Their RNA Inhabitants Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses
2016Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya YutinAbstract:Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolu-tionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales, ” adenoviruses, and Virophages from a group of large virus-like transposons known as Polintons (Mav-ericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polin-toviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, Virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales, ” and linearmitochondrial and cytoplasmic plasmids.We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provide
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a novel group of diverse polinton like viruses discovered by metagenome analysis
BMC Biology, 2015Co-Authors: Natalya Yutin, Mart Krupovic, Vladimir V Kapitonov, Sofiya Shevchenko, Eugene V. KooninAbstract:The rapidly growing metagenomic databases provide increasing opportunities for computational discovery of new groups of organisms. Identification of new viruses is particularly straightforward given the comparatively small size of viral genomes, although fast evolution of viruses complicates the analysis of novel sequences. Here we report the metagenomic discovery of a distinct group of diverse viruses that are distantly related to the eukaryotic virus-like transposons of the Polinton superfamily. The sequence of the putative major capsid protein (MCP) of the unusual linear Virophage associated with Phaeocystis globosa virus (PgVV) was used as a bait to identify potential related viruses in metagenomic databases. Assembly of the contigs encoding the PgVV MCP homologs followed by comprehensive sequence analysis of the proteins encoded in these contigs resulted in the identification of a large group of Polinton-like viruses (PLV) that resemble Polintons (polintoviruses) and Virophages in genome size, and share with them a conserved minimal morphogenetic module that consists of major and minor capsid proteins and the packaging ATPase. With a single exception, the PLV lack the retrovirus-type integrase that is encoded in the genomes of all Polintons and the Mavirus group of Virophages. However, some PLV encode a newly identified tyrosine recombinase-integrase that is common in bacteria and bacteriophages and is also found in the Organic Lake Virophage group. Although several PLV genomes and individual genes are integrated into algal genomes, it appears likely that most of the PLV are viruses. Given the absence of protease and retrovirus-type integrase, the PLV could resemble the ancestral polintoviruses that evolved from bacterial tectiviruses. Apart from the conserved minimal morphogenetic module, the PLV widely differ in their genome complements but share a gene network with Polintons and Virophages, suggestive of multiple gene exchanges within a shared gene pool. The discovery of PLV substantially expands the emerging class of eukaryotic viruses and transposons that also includes Polintons and Virophages. This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered.
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a new family of hybrid Virophages from an animal gut metagenome
Biology Direct, 2015Co-Authors: Natalya Yutin, Vladimir V Kapitonov, Eugene V. KooninAbstract:Search of metagenomics sequence databases for homologs of Virophage capsid proteins resulted in the discovery of a new family of Virophages in the sheep rumen metagenome. The genomes of the rumen Virophages (RVP) encode a typical Virophage major capsid protein, ATPase and protease combined with a Polinton-type, protein primed family B DNA polymerase. The RVP genomes appear to be linear molecules, with terminal inverted repeats. Thus, the RVP seem to represent Virophage-Polinton hybrids that are likely capable of formation of infectious virions. Virion proteins of mimiviruses were detected in the same metagenomes as the RVP suggesting that the Virophages of the new family parasitize on giant viruses that infect protist inhabitants of the rumen.
Natalya Yutin - One of the best experts on this subject based on the ideXlab platform.
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Genome and Environmental Activity of a Chrysochromulina parva Virus and Its Virophages
Frontiers Media S.A., 2019Co-Authors: Joshua M. A. Stough, Natalya Yutin, Eugene V. Koonin, Yuri V. Chaban, Mohammed Moniruzzaman, Eric R. Gann, Helena L. Pound, Morgan M. Steffen, Jenna N. Black, Steven W. WilhelmAbstract:Some giant viruses are ecological agents that are predicted to be involved in the top-down control of single-celled eukaryotic algae populations in aquatic ecosystems. Despite an increased interest in giant viruses since the discovery and characterization of Mimivirus and other viral giants, little is known about their physiology and ecology. In this study, we characterized the genome and functional potential of a giant virus that infects the freshwater haptophyte Chrysochromulina parva, originally isolated from Lake Ontario. This virus, CpV-BQ2, is a member of the nucleo-cytoplasmic large DNA virus (NCLDV) group and possesses a 437 kb genome encoding 503 ORFs with a GC content of 25%. Phylogenetic analyses of core NCLDV genes place CpV-BQ2 amongst the emerging group of algae-infecting Mimiviruses informally referred to as the “extended Mimiviridae,” making it the first virus of this group to be isolated from a freshwater ecosystem. During genome analyses, we also captured and described the genomes of three distinct Virophages that co-occurred with CpV-BQ2 and likely exploit CpV for their own replication. These Virophages belong to the polinton-like viruses (PLV) group and encompass 19–23 predicted genes, including all of the core PLV genes as well as several genes implicated in genome modifications. We used the CpV-BQ2 and Virophage reference sequences to recruit reads from available environmental metatranscriptomic data to estimate their activity in fresh waters. We observed moderate recruitment of both virus and Virophage transcripts in samples obtained during Microcystis aeruginosa blooms in Lake Erie and Lake Tai, China in 2013, with a spike in activity in one sample. Virophage transcript abundance for two of the three isolates strongly correlated with that of the CpV-BQ2. Together, the results highlight the importance of giant viruses in the environment and establish a foundation for future research on the physiology and ecology CpV-BQ2 as a model system for algal Mimivirus dynamics in freshwaters
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Data_Sheet_1_Genome and Environmental Activity of a Chrysochromulina parva Virus and Its Virophages.PDF
2019Co-Authors: Joshua M. A. Stough, Natalya Yutin, Eugene V. Koonin, Yuri V. Chaban, Mohammed Moniruzzaman, Eric R. Gann, Helena L. Pound, Morgan M. Steffen, Jenna N. Black, Steven W. WilhelmAbstract:Some giant viruses are ecological agents that are predicted to be involved in the top-down control of single-celled eukaryotic algae populations in aquatic ecosystems. Despite an increased interest in giant viruses since the discovery and characterization of Mimivirus and other viral giants, little is known about their physiology and ecology. In this study, we characterized the genome and functional potential of a giant virus that infects the freshwater haptophyte Chrysochromulina parva, originally isolated from Lake Ontario. This virus, CpV-BQ2, is a member of the nucleo-cytoplasmic large DNA virus (NCLDV) group and possesses a 437 kb genome encoding 503 ORFs with a GC content of 25%. Phylogenetic analyses of core NCLDV genes place CpV-BQ2 amongst the emerging group of algae-infecting Mimiviruses informally referred to as the “extended Mimiviridae,” making it the first virus of this group to be isolated from a freshwater ecosystem. During genome analyses, we also captured and described the genomes of three distinct Virophages that co-occurred with CpV-BQ2 and likely exploit CpV for their own replication. These Virophages belong to the polinton-like viruses (PLV) group and encompass 19–23 predicted genes, including all of the core PLV genes as well as several genes implicated in genome modifications. We used the CpV-BQ2 and Virophage reference sequences to recruit reads from available environmental metatranscriptomic data to estimate their activity in fresh waters. We observed moderate recruitment of both virus and Virophage transcripts in samples obtained during Microcystis aeruginosa blooms in Lake Erie and Lake Tai, China in 2013, with a spike in activity in one sample. Virophage transcript abundance for two of the three isolates strongly correlated with that of the CpV-BQ2. Together, the results highlight the importance of giant viruses in the environment and establish a foundation for future research on the physiology and ecology CpV-BQ2 as a model system for algal Mimivirus dynamics in freshwaters.
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ANNALS OF THE NEW YORK ACADEMY OF SCIENCES Issue:DNA Habitats and Their RNA Inhabitants Evolution of double-stranded DNA viruses of eukaryotes: from bacteriophages to transposons to giant viruses
2016Co-Authors: Eugene V. Koonin, Mart Krupovic, Natalya YutinAbstract:Diverse eukaryotes including animals and protists are hosts to a broad variety of viruses with double-stranded (ds) DNA genomes, from the largest known viruses, such as pandoraviruses and mimiviruses, to tiny polyomaviruses. Recent comparative genomic analyses have revealed many evolutionary connections between dsDNA viruses of eukaryotes, bacteriophages, transposable elements, and linear DNA plasmids. These findings provide an evolu-tionary scenario that derives several major groups of eukaryotic dsDNA viruses, including the proposed order “Megavirales, ” adenoviruses, and Virophages from a group of large virus-like transposons known as Polintons (Mav-ericks). The Polintons have been recently shown to encode two capsid proteins, suggesting that these elements lead a dual lifestyle with both a transposon and a viral phase and should perhaps more appropriately be named polin-toviruses. Here, we describe the recently identified evolutionary relationships between bacteriophages of the family Tectiviridae, polintoviruses, adenoviruses, Virophages, large and giant DNA viruses of eukaryotes of the proposed order “Megavirales, ” and linearmitochondrial and cytoplasmic plasmids.We outline an evolutionary scenario under which the polintoviruses were the first group of eukaryotic dsDNA viruses that evolved from bacteriophages and became the ancestors of most large DNA viruses of eukaryotes and a variety of other selfish elements. Distinct lines of origin are detectable only for herpesviruses (from a different bacteriophage root) and polyoma/papillomaviruses (from single-stranded DNA viruses and ultimately from plasmids). Phylogenomic analysis of giant viruses provide
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a novel group of diverse polinton like viruses discovered by metagenome analysis
BMC Biology, 2015Co-Authors: Natalya Yutin, Mart Krupovic, Vladimir V Kapitonov, Sofiya Shevchenko, Eugene V. KooninAbstract:The rapidly growing metagenomic databases provide increasing opportunities for computational discovery of new groups of organisms. Identification of new viruses is particularly straightforward given the comparatively small size of viral genomes, although fast evolution of viruses complicates the analysis of novel sequences. Here we report the metagenomic discovery of a distinct group of diverse viruses that are distantly related to the eukaryotic virus-like transposons of the Polinton superfamily. The sequence of the putative major capsid protein (MCP) of the unusual linear Virophage associated with Phaeocystis globosa virus (PgVV) was used as a bait to identify potential related viruses in metagenomic databases. Assembly of the contigs encoding the PgVV MCP homologs followed by comprehensive sequence analysis of the proteins encoded in these contigs resulted in the identification of a large group of Polinton-like viruses (PLV) that resemble Polintons (polintoviruses) and Virophages in genome size, and share with them a conserved minimal morphogenetic module that consists of major and minor capsid proteins and the packaging ATPase. With a single exception, the PLV lack the retrovirus-type integrase that is encoded in the genomes of all Polintons and the Mavirus group of Virophages. However, some PLV encode a newly identified tyrosine recombinase-integrase that is common in bacteria and bacteriophages and is also found in the Organic Lake Virophage group. Although several PLV genomes and individual genes are integrated into algal genomes, it appears likely that most of the PLV are viruses. Given the absence of protease and retrovirus-type integrase, the PLV could resemble the ancestral polintoviruses that evolved from bacterial tectiviruses. Apart from the conserved minimal morphogenetic module, the PLV widely differ in their genome complements but share a gene network with Polintons and Virophages, suggestive of multiple gene exchanges within a shared gene pool. The discovery of PLV substantially expands the emerging class of eukaryotic viruses and transposons that also includes Polintons and Virophages. This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered.
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a new family of hybrid Virophages from an animal gut metagenome
Biology Direct, 2015Co-Authors: Natalya Yutin, Vladimir V Kapitonov, Eugene V. KooninAbstract:Search of metagenomics sequence databases for homologs of Virophage capsid proteins resulted in the discovery of a new family of Virophages in the sheep rumen metagenome. The genomes of the rumen Virophages (RVP) encode a typical Virophage major capsid protein, ATPase and protease combined with a Polinton-type, protein primed family B DNA polymerase. The RVP genomes appear to be linear molecules, with terminal inverted repeats. Thus, the RVP seem to represent Virophage-Polinton hybrids that are likely capable of formation of infectious virions. Virion proteins of mimiviruses were detected in the same metagenomes as the RVP suggesting that the Virophages of the new family parasitize on giant viruses that infect protist inhabitants of the rumen.
Matthias G. Fischer - One of the best experts on this subject based on the ideXlab platform.
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endogenous Virophages populate the genomes of a marine heterotrophic flagellate
bioRxiv, 2020Co-Authors: Thomas Hackl, Sarah Duponchel, Karina Barenhoff, Alexa Weinmann, Matthias G. FischerAbstract:Abstract Endogenous viral elements (EVEs) are frequently found in eukaryotic genomes, yet their integration dynamics and biological functions remain largely unknown. Unlike most other eukaryotic DNA viruses, the Virophage mavirus integrates efficiently into the nuclear genome of its host, the marine heterotrophic flagellate Cafeteria burkhardae. Mavirus EVEs can reactivate upon superinfection with the lytic giant virus CroV and may act as an adaptive antiviral defense system, because mavirus increases host population survival during a coinfection with CroV. However, the prevalence of endogenous Virophages in natural flagellate populations has not been explored. Here we report dozens of endogenous mavirus-like elements (EMALEs) in the nuclear genomes of four C. burkhardae strains. EMALEs were typically 20 kilobase pairs long and constituted 0.7% to 1.8% of each host genome. We analyzed 33 fully assembled EMALEs that fell into two main clusters and eight types based on GC-content, nucleotide similarity, and coding potential. Inter-strain comparison showed conservation of some EMALE insertion loci, whereas the majority of integration sites were unique to a given host strain. We also describe a group of tyrosine recombinase retrotransposons, some of which exhibited a strong preference for integration into EMALEs and represent yet another layer of parasitism in this microbial system. Our findings show that Virophages are common, diverse, and dynamic genome components of the marine protist C. burkhardae, which implies important eco-evolutionary roles for these enigmatic viruses.
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the dual lifestyle of genome integrating Virophages in protists
Annals of the New York Academy of Sciences, 2019Co-Authors: Monica Berjonotero, Anna Koslova, Matthias G. FischerAbstract:DNA viruses with efficient host genome integration capability were unknown in eukaryotes until recently. The discovery of Virophages, satellite-like DNA viruses that depend on lytic giant viruses that infect protists, revealed a genetically diverse group of viruses with high genome mobility. Virophages can act as strong inhibitors of their associated giant viruses, and the resulting beneficial effects on their unicellular hosts resemble a population-based antiviral defense mechanism. By comparing various aspects of genome-integrating Virophages, in particular the Virophage mavirus, with other mobile genetic elements and parasite-derived defense mechanisms in eukaryotes and prokaryotes, we show that Virophages share many features with other host-parasite systems. Yet, the dual lifestyle exhibited by mavirus remains unprecedented among eukaryotic DNA viruses, with potentially far-reaching ecological and evolutionary consequences for the host.
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Proposed GV and Virophage infection cycle in a eukaryotic host cell.
2019Co-Authors: Sarah Duponchel, Matthias G. FischerAbstract:Some GV capsids (e.g., mimivirus) are covered in fibers that allow co-entry of Virophages (e.g., Sputnik) by phagocytosis. Other Virophages such as mavirus enter cells by receptor-mediated endocytosis. After opening of the GV capsid and fusion of the internal GV membrane with the phagosomal or cytoplasmic membrane, the GV core is released into the cytoplasm and develops into the viral factory. The Virophage genome is targeted to the factory, where the GV-encoded transcriptase complex activates Virophage genes during the late phase of GV infection. Virophage genome replication is catalyzed by Virophage-encoded DNA polymerases and helicases, and Virophage particles are assembled within or near the GV factory and are released upon cell lysis. Virophage replication can inhibit GV production. Alternatively, the mavirus genome is able to integrate into the nuclear host genome independently of a GV. The otherwise transcriptionally silent proVirophage genes can be activated during infection with a compatible GV, leading to the production of Virophage particles in the GV factory. GV, giant virus.
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Genome organization and capsid shape of cultured Virophages.
2019Co-Authors: Sarah Duponchel, Matthias G. FischerAbstract:(A) Genome representation of the Virophages Sputnik, Zamilon, and mavirus. Homologous genes are colored identically. (B) Electron microscopy images depicting capsids of giant viruses and their associated Virophages. (Left) CroV (dark) and mavirus (light); negative stain EM courtesy of U. Mersdorf, MPI for Medical Research, Germany. (Middle) Megavirus vitis (with a visible stargate structure) and Zamilon vitis (inset); negative stain EM courtesy of C. Abergel, Aix-Marseille Université, France. (Right) Acanthamoeba polyphaga mimivirus with two Sputnik virus particles (arrows); thin-section EM courtesy of J.Y. Bou Khalil and B. La Scola, IHU Mediterranée Infection, France. Note that all three Virophages have similar capsid sizes but are shown here at different magnifications. EM, electron microscopy; CroV, Cafeteria roenbergensis virus; TIR, terminal inverted repeat.
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capsid protein structure self assembly and processing reveal morphogenesis of the marine Virophage mavirus
Proceedings of the National Academy of Sciences of the United States of America, 2018Co-Authors: Diana Born, Matthias G. Fischer, Lukas Reuter, Ulrike Mersdorf, Melanie Mueller, Anton Meinhart, Jochen ReinsteinAbstract:Virophages have the unique property of parasitizing giant viruses within unicellular hosts. Little is understood about how they form infectious virions in this tripartite interplay. We provide mechanistic insights into assembly and maturation of mavirus, a marine Virophage, by combining structural and stability studies on capsomers, virus-like particles (VLPs), and native virions. We found that the mavirus protease processes the double jelly-roll (DJR) major capsid protein (MCP) at multiple C-terminal sites and that these sites are conserved among Virophages. Mavirus MCP assembled in Escherichia coli in the absence and presence of penton protein, forming VLPs with defined size and shape. While quantifying VLPs in E. coli lysates, we found that full-length rather than processed MCP is the competent state for capsid assembly. Full-length MCP was thermally more labile than truncated MCP, and crystal structures of both states indicate that full-length MCP has an expanded DJR core. Thus, we propose that the MCP C-terminal domain serves as a scaffolding domain by adding strain on MCP to confer assembly competence. Mavirus protease processed MCP more efficiently after capsid assembly, which provides a regulation mechanism for timing capsid maturation. By analogy to Sputnik and adenovirus, we propose that MCP processing renders mavirus particles infection competent by loosening interactions between genome and capsid shell and destabilizing pentons for genome release into host cells. The high structural similarity of mavirus and Sputnik capsid proteins together with conservation of protease and MCP processing suggest that assembly and maturation mechanisms described here are universal for Virophages.