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1
Aylward, Frank O., Mohammad Moniruzzaman, Anh D. Ha, and Eugene V. Koonin. "A phylogenomic framework for charting the diversity and evolution of giant viruses." PLOS Biology 19, no. 10 (October 27, 2021): e3001430. http://dx.doi.org/10.1371/journal.pbio.3001430.
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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.
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Gaïa, Morgan, and Patrick Forterre. "From Mimivirus to Mirusvirus: The Quest for Hidden Giants." Viruses 15, no. 8 (August 17, 2023): 1758. http://dx.doi.org/10.3390/v15081758.
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Our perception of viruses has been drastically evolving since the inception of the field of virology over a century ago. In particular, the discovery of giant viruses from the Nucleocytoviricota phylum marked a pivotal moment. Their previously concealed diversity and abundance unearthed an unprecedented complexity in the virus world, a complexity that called for new definitions and concepts. These giant viruses underscore the intricate interactions that unfold over time between viruses and their hosts, and are themselves suspected to have played a significant role as a driving force in the evolution of eukaryotes since the dawn of this cellular domain. Whether they possess exceptional relationships with their hosts or whether they unveil the actual depths of evolutionary connections between viruses and cells otherwise hidden in smaller viruses, the attraction giant viruses exert on the scientific community and beyond continues to grow. Yet, they still hold surprises. Indeed, the recent identification of mirusviruses connects giant viruses to herpesviruses, each belonging to distinct viral realms. This discovery substantially broadens the evolutionary landscape of Nucleocytoviricota. Undoubtedly, the years to come will reveal their share of surprises.
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de Souza, Fernanda Gil, Jônatas Santos Abrahão, and Rodrigo Araújo Lima Rodrigues. "Comparative Analysis of Transcriptional Regulation Patterns: Understanding the Gene Expression Profile in Nucleocytoviricota." Pathogens 10, no. 8 (July 24, 2021): 935. http://dx.doi.org/10.3390/pathogens10080935.
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The nucleocytoplasmic large DNA viruses (NCLDV) possess unique characteristics that have drawn the attention of the scientific community, and they are now classified in the phylum Nucleocytoviricota. They are characterized by sharing many genes and have their own transcriptional apparatus, which provides certain independence from their host’s machinery. Thus, the presence of a robust transcriptional apparatus has raised much discussion about the evolutionary aspects of these viruses and their genomes. Understanding the transcriptional process in NCLDV would provide information regarding their evolutionary history and a better comprehension of the biology of these viruses and their interaction with hosts. In this work, we reviewed NCLDV transcription and performed a comparative functional analysis of the groups of genes expressed at different times of infection of representatives of six different viral families of giant viruses. With this analysis, it was possible to observe a temporal profile of their gene expression and set of genes activated in specific phases throughout the multiplication cycle as a common characteristic of this group. Due to the lack of information regarding the transcriptional regulation process of this group of pathogens, we sought to provide information that contributes to and opens up the field for transcriptional studies of other viruses belonging to Nucleocytoviricota.
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Rodrigues, Rodrigo AL, Fernanda G. de Souza, Bruna L. de Azevedo, Lorena CF da Silva, and Jônatas S. Abrahão. "The morphogenesis of different giant viruses as additional evidence for a common origin of Nucleocytoviricota." Current Opinion in Virology 49 (August 2021): 102–10. http://dx.doi.org/10.1016/j.coviro.2021.05.004.
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Ruiz Martínez, Eliana, Dean A. Mckeown, Declan C. Schroeder, Gunnar Thuestad, Kjersti Sjøtun, Ruth-Anne Sandaa, Aud Larsen, and Ingunn Alne Hoell. "Phaeoviruses Present in Cultured and Natural Kelp Species, Saccharina latissima and Laminaria hyperborea (Phaeophyceae, Laminariales), in Norway." Viruses 15, no. 12 (November 28, 2023): 2331. http://dx.doi.org/10.3390/v15122331.
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Phaeoviruses (Phycodnaviridae) are large icosahedral viruses in the phylum Nucleocytoviricota with dsDNA genomes ranging from 160 to 560 kb, infecting multicellular brown algae (Phaeophyceae). The phaeoviral host range is broader than expected, not only infecting algae from the Ectocarpales but also from the Laminariales order. However, despite phaeoviral infections being reported globally, Norwegian kelp species have not been screened. A molecular analysis of cultured and wild samples of two economically important kelp species in Norway (Saccharina latissima and Laminaria hyperborea) revealed that phaeoviruses are recurrently present along the Norwegian coast. We found the viral prevalence in S. latissima to be significantly higher at the present time compared to four years ago. We also observed regional differences within older samples, in which infections were significantly lower in northern areas than in the south or the fjords. Moreover, up to three different viral sequences were found in the same algal individual, one of which does not belong to the Phaeovirus genus and has never been reported before. This master variant therefore represents a putative new member of an unclassified phycodnavirus genus.
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de Oliveira, Ellen Gonçalves, João Victor Rodrigues Pessoa Carvalho, Bruna Barbosa Botelho, Clécio Alonso da Costa Filho, Lethícia Ribeiro Henriques, Bruna Luiza de Azevedo, and Rodrigo Araújo Lima Rodrigues. "Giant Viruses as a Source of Novel Enzymes for Biotechnological Application." Pathogens 11, no. 12 (December 1, 2022): 1453. http://dx.doi.org/10.3390/pathogens11121453.
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The global demand for industrial enzymes has been increasing in recent years, and the search for new sources of these biological products is intense, especially in microorganisms. Most known viruses have limited genetic machinery and, thus, have been overlooked by the enzyme industry for years. However, a peculiar group of viruses breaks this paradigm. Giant viruses of the phylum Nucleocytoviricota infect protists (i.e., algae and amoebae) and have complex genomes, reaching up to 2.7 Mb in length and encoding hundreds of genes. Different giant viruses have robust metabolic machinery, especially those in the Phycodnaviridae and Mimiviridae families. In this review, we present some peculiarities of giant viruses that infect protists and discuss why they should be seen as an outstanding source of new enzymes. We revisited the genomes of representatives of different groups of giant viruses and put together information about their enzymatic machinery, highlighting several genes to be explored in biotechnology involved in carbohydrate metabolism, DNA replication, and RNA processing, among others. Finally, we present additional evidence based on structural biology using chitinase as a model to reinforce the role of giant viruses as a source of novel enzymes for biotechnological application.
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Claverie, Jean-Michel. "Fundamental Difficulties Prevent the Reconstruction of the Deep Phylogeny of Viruses." Viruses 12, no. 10 (October 6, 2020): 1130. http://dx.doi.org/10.3390/v12101130.
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The extension of virology beyond its traditional medical, veterinary, or agricultural applications, now called environmental virology, has shown that viruses are both the most numerous and diverse biological entities on Earth. In particular, virus isolations from unicellular eukaryotic hosts (heterotrophic and photosynthetic protozoans) revealed numerous viral types previously unexpected in terms of virion structure, gene content, or mode of replication. Complemented by large-scale metagenomic analyses, these discoveries have rekindled interest in the enigma of the origin of viruses, for which a description encompassing all their diversity remains not available. Several laboratories have repeatedly tackled the deep reconstruction of the evolutionary history of viruses, using various methods of molecular phylogeny applied to the few shared “core” genes detected in certain virus groups (e.g., the Nucleocytoviricota). Beyond the practical difficulties of establishing reliable homology relationships from extremely divergent sequences, I present here conceptual arguments highlighting several fundamental limitations plaguing the reconstruction of the deep evolutionary history of viruses, and even more the identification of their unique or multiple origin(s). These arguments also underline the risk of establishing premature high level viral taxonomic classifications. Those limitations are direct consequences of the random mechanisms governing the reductive/retrogressive evolution of all obligate intracellular parasites.
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Kukovetz, Kerri, Brigitte Hertel, Christopher R. Schvarcz, Andrea Saponaro, Mirja Manthey, Ulrike Burk, Timo Greiner, et al. "A Functional K+ Channel from Tetraselmis Virus 1, a Member of the Mimiviridae." Viruses 12, no. 10 (September 29, 2020): 1107. http://dx.doi.org/10.3390/v12101107.
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Potassium ion (K+) channels have been observed in diverse viruses that infect eukaryotic marine and freshwater algae. However, experimental evidence for functional K+ channels among these alga-infecting viruses has thus far been restricted to members of the family Phycodnaviridae, which are large, double-stranded DNA viruses within the phylum Nucleocytoviricota. Recent sequencing projects revealed that alga-infecting members of Mimiviridae, another family within this phylum, may also contain genes encoding K+ channels. Here we examine the structural features and the functional properties of putative K+ channels from four cultivated members of Mimiviridae. While all four proteins contain variations of the conserved selectivity filter sequence of K+ channels, structural prediction algorithms suggest that only two of them have the required number and position of two transmembrane domains that are present in all K+ channels. After in vitro translation and reconstitution of the four proteins in planar lipid bilayers, we confirmed that one of them, a 79 amino acid protein from the virus Tetraselmis virus 1 (TetV-1), forms a functional ion channel with a distinct selectivity for K+ over Na+ and a sensitivity to Ba2+. Thus, virus-encoded K+ channels are not limited to Phycodnaviridae but also occur in the members of Mimiviridae. The large sequence diversity among the viral K+ channels implies multiple events of lateral gene transfer.
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Kyndt, Elliot C., and John A. Kyndt. "Illumina Short-Read Sequencing of the Mitogenomes of Novel Scarites subterraneus Isolates Allows for Taxonomic Refinement of the Genus Scarites Fabricius 1775, within the Carabidae Family." Insects 13, no. 2 (February 11, 2022): 190. http://dx.doi.org/10.3390/insects13020190.
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We sequenced the complete mitogenomes, 18S and 28S rRNA of two new Scarites isolates, collected in Eastern Nebraska and Northern Arkansas (US). Based on molecular sequence data comparison and morphological characteristics, the new isolates were identified as a subspecies of Scarites subterraneus Fabricius 1775, for which we propose the subspecies names ‘nebraskensis’ and ‘arkansensis’. The new 18S and 28S rRNA sequences were found to be 99% and 98% identical to Scarites subterraneus. There are no other Scarites 18S or 28S rRNA sequences in the Genbank database, however, phylogenetic analysis of the Cox1 genes showed S. vicinus Chaudoir, 1843, and S. aterrimus Morawitz, 1863, as the closest relatives. This is the first report of a mitogenome for S. subterraneus, and only the second mitogenome for that genus. The nucleotide sequence identity between the mitogenomes of the two isolates is 98.8%, while the earlier sequenced S. buparius Forster 1771 mitogenome is more distantly related, with only 90% (to ssp. nebraskensis) and 89% (to ssp. arkansensis) overall nucleotide sequence identity. These new mitogenomes, and their phylogenetic analysis, firmly establish the position of Scarites on the Carabidae family tree and further refine the genus. In addition to the molecular data provided for the Scarites species, this approach also allowed us to identify bacterial and viral signatures for Providencia, Myroides, Spiroplasma, and a giant Nucleocytoviricota virus, associated with the Scarites species. We hereby present a simple and efficient protocol for identification and phylogenetic analysis of Scarites, that is applicable to other Coleoptera, based on total DNA extraction and Illumina short-read Next-Gen sequencing.
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Bernadus, Janno Berty Bradly, Jantje Pelealu, Grace Debbie Kandou, Arthur Gehart Pinaria, Juliet Merry Eva Mamahit, and Trina Ekawati Tallei. "Metagenomic Insight into the Microbiome and Virome Associated with Aedes aegypti Mosquitoes in Manado (North Sulawesi, Indonesia)." Infectious Disease Reports 15, no. 5 (September 11, 2023): 549–63. http://dx.doi.org/10.3390/idr15050054.
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The aim of this study was to investigate the microbial diversity encompassing bacteria, fungi, and viruses within the composite microbial community associated with Aedes aegypti mosquitoes in Manado, Indonesia, using a whole-genome shotgun metagenomics approach. Female mosquitoes were collected and grouped into pools of 50 individuals, from which genomic DNA (gDNA) and RNA were extracted separately. Whole-genome shotgun metagenomics were performed on gDNA samples. The bioinformatics analysis encompassed quality assessment, taxonomic classification, and visualization. The evaluation of the microbial community entailed an assessment of taxa abundance and diversity using Kraken version 2.1.2. The study delineated the prevalence of dominant bacterial phyla, including Proteobacteria, with varying abundance of Firmicutes, Bacteroidota, and Actinobacteria, and notable occurrence of Tenericutes. Furthermore, the presence of the fungal phylum Ascomycota was also detected. Among the identified barcodes, Barcode04 emerged as the most abundant and diverse, while Barcode06 exhibited greater evenness. Barcode03, 05, and 07 displayed moderate richness and diversity. Through an analysis of the relative abundance, a spectrum of viruses within Ae. aegypti populations was unveiled, with Negarnaviricota constituting the most prevalent phylum, followed by Nucleocytoviricota, Uroviricota, Artverviricota, Kitrinoviricota, Peploviricota, Phixviricota, and Cossaviricota. The presence of Negarnaviricota viruses raises pertinent public health concerns. The presence of other viral phyla underscores the intricate nature of virus–mosquito interactions. The analysis of viral diversity provides valuable insights into the range of viruses carried by Ae. aegypti. The community exhibits low biodiversity, with a few dominant species significantly influencing its composition. This has implications for healthcare and ecological management, potentially simplifying control measures but also posing risks if the dominant species are harmful. This study enriches our comprehension of the microbiome and virome associated with Ae. aegypti mosquitoes, emphasizing the importance of further research to fully comprehend their ecological significance and impact on public health. The findings shed light on the microbial ecology of Ae. aegypti, offering potential insights into mosquito biology, disease transmission, and strategies for vector control. Future studies should endeavor to establish specific associations with Ae. aegypti, elucidate the functional roles of the identified microbial and viral species, and investigate their ecological implications.
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Guglielmini, Julien, Morgan Gaia, Violette Da Cunha, Alexis Criscuolo, Mart Krupovic, and Patrick Forterre. "Viral origin of eukaryotic type IIA DNA topoisomerases." Virus Evolution, October 8, 2022. http://dx.doi.org/10.1093/ve/veac097.
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Abstract Type II DNA topoisomerases of the family A (Topo IIA) are present in all bacteria (DNA gyrase) and eukaryotes. In eukaryotes, they play a major role in transcription, DNA replication, chromosome segregation and modulation of chromosome architecture. The origin of eukaryotic Topo IIA remains mysterious since they are very divergent from their bacterial homologues and have no orthologues in Archaea. Interestingly, eukaryotic Topo IIA have close homologues in viruses of the phylum Nucleocytoviricota, an expansive assemblage of large and giant viruses formerly known as the nucleocytoplasmic large DNA viruses (NCLDV). Topo IIA are also encoded by some bacterioviruses of the class Caudoviricetes (tailed bacteriophages). To elucidate the origin of the eukaryotic Topo IIA, we performed in-depth phylogenetic analyses combining viral and cellular Topo IIA homologs. Topo IIA encoded by bacteria and eukaryotes form two monophyletic groups nested within Topo IIA encoded by Caudoviricetes and Nucleocytoviricota, respectively. Importantly, Nucleocytoviricota remained well separated from eukaryotes after removing both bacteria and Caudoviricetes from the dataset, indicating that the separation of Nucleocytoviricota and eukaryotes is probably not due to long branch attraction artefact. The topology of our tree suggests that the eukaryotic Topo IIA was probably acquired from an ancestral member of the Nucleocytoviricota of the class Megaviricetes, before the emergence of the last eukaryotic common ancestor (LECA). This result further highlights a key role of these viruses in eukaryogenesis and suggests that early proto-eukaryotes used a Topo IIB instead of a Topo IIA for solving their DNA topological problems
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Krupovic, Mart, Natalya Yutin, and Eugene Koonin. "Evolution of a major virion protein of the giant pandoraviruses from an inactivated bacterial glycoside hydrolase." Virus Evolution 6, no. 2 (July 1, 2020). http://dx.doi.org/10.1093/ve/veaa059.
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Abstract The diverse viruses in the phylum Nucleocytoviricota (also known as NLCDVs, Nucleo-cytoplasmic Large DNA Viruses) typically possess large icosahedral virions. However, in several families of Nucleocytoviricota, the icosahedral capsid was replaced by irregular particle shapes, most notably, the amphora-like virions of pandoraviruses and pithoviruses, the largest known virus particles in the entire virosphere. Pandoraviruses appear to be the most highly derived viruses in this phylum because their evolution involved not only the change in the virion shape, but also, the actual loss of the gene encoding double-jelly roll major capsid protein (DJR MCP), the main building block of icosahedral capsids in this virus assemblage. Instead, pandoravirus virions are built of unrelated abundant proteins. Here we show that the second most abundant virion protein of pandoraviruses, major virion protein 2 (MVP2), evolved from an inactivated derivative of a bacterial glycoside hydrolase of the GH16 family. The ancestral form of MVP2 was apparently acquired early in the evolution of the Nucleocytoviricota, to become a minor virion protein. After a duplication in the common ancestor of pandoraviruses and molliviruses, one of the paralogs displaces DJR MCP in pandoraviruses, conceivably, opening the way for a major increase in the size of the virion and the genome. Exaptation of a carbohydrate-binding protein for the function of the MVP is a general trend in virus evolution and might underlie the transformation of the virion shape in other groups of the Nucleocytoviricota as well.
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Truchon, Alexander R., Emily E. Chase, Eric R. Gann, Mohammad Moniruzzaman, Brooke A. Creasey, Frank O. Aylward, Chuan Xiao, Christopher J. Gobler, and Steven W. Wilhelm. "Kratosvirus quantuckense: the history and novelty of an algal bloom disrupting virus and a model for giant virus research." Frontiers in Microbiology 14 (November 30, 2023). http://dx.doi.org/10.3389/fmicb.2023.1284617.
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Since the discovery of the first “giant virus,” particular attention has been paid toward isolating and culturing these large DNA viruses through Acanthamoeba spp. bait systems. While this method has allowed for the discovery of plenty novel viruses in the Nucleocytoviricota, environmental -omics-based analyses have shown that there is a wealth of diversity among this phylum, particularly in marine datasets. The prevalence of these viruses in metatranscriptomes points toward their ecological importance in nutrient turnover in our oceans and as such, in depth study into non-amoebal Nucleocytoviricota should be considered a focal point in viral ecology. In this review, we report on Kratosvirus quantuckense (née Aureococcus anophagefferens Virus), an algae-infecting virus of the Imitervirales. Current systems for study in the Nucleocytoviricota differ significantly from this virus and its relatives, and a litany of trade-offs within physiology, coding potential, and ecology compared to these other viruses reveal the importance of K. quantuckense. Herein, we review the research that has been performed on this virus as well as its potential as a model system for algal-virus interactions.
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Zhang, Ruixuan, Hisashi Endo, Masaharu Takemura, and Hiroyuki Ogata. "RNA Sequencing of Medusavirus Suggests Remodeling of the Host Nuclear Environment at an Early Infection Stage." Microbiology Spectrum 9, no. 2 (October 31, 2021). http://dx.doi.org/10.1128/spectrum.00064-21.
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Zhang, Ruixuan, Masaharu Takemura, Kazuyoshi Murata, and Hiroyuki Ogata. "“Mamonoviridae”, a proposed new family of the phylum Nucleocytoviricota." Archives of Virology 168, no. 3 (February 5, 2023). http://dx.doi.org/10.1007/s00705-022-05633-1.
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Queiroz, Victória F., João Victor R. P. Carvalho, Fernanda G. de Souza, Maurício T. Lima, Juliane D. Santos, Kamila L. S. Rocha, Danilo B. de Oliveira, et al. "Analysis of the Genomic Features and Evolutionary History of Pithovirus-Like Isolates Reveals Two Major Divergent Groups of Viruses." Journal of Virology, July 3, 2023. http://dx.doi.org/10.1128/jvi.00411-23.
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Giant viruses that infect amoebae form a monophyletic group named the phylum Nucleocytoviricota . Despite being genomically and morphologically very diverse, the taxonomic categories of some clades that form this phylum are not yet well established.
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Hosokawa, Nao, Haruna Takahashi, Keita Aoki, and Masaharu Takemura. "Draft Genome Sequence of Pandoravirus japonicus Isolated from the Sabaishi River, Niigata, Japan." Microbiology Resource Announcements 10, no. 19 (May 13, 2021). http://dx.doi.org/10.1128/mra.00365-21.
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“ Pandoraviridae ” is a proposed family of the phylum Nucleocytoviricota . Its features include an amphora-shaped capsid and the largest genome among all viruses. We report the isolation and genome sequencing of a new member of this family, named Pandoravirus japonicus , the third strain discovered in Japan.
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Bhattacharjee, Ananda S., Frederik Schulz, Tanja Woyke, Beth N. Orcutt, and Joaquín Martínez Martínez. "Genomics discovery of giant fungal viruses from subsurface oceanic crustal fluids." ISME Communications 3, no. 1 (February 3, 2023). http://dx.doi.org/10.1038/s43705-022-00210-8.
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AbstractThe oceanic igneous crust is a vast reservoir for microbial life, dominated by diverse and active bacteria, archaea, and fungi. Archaeal and bacterial viruses were previously detected in oceanic crustal fluids at the Juan de Fuca Ridge (JdFR). Here we report the discovery of two eukaryotic Nucleocytoviricota genomes from the same crustal fluids by sorting and sequencing single virions. Both genomes have a tRNATyr gene with an intron (20 bps) at the canonical position between nucleotide 37 and 38, a common feature in eukaryotic and archaeal tRNA genes with short introns (<100 bps), and fungal genes acquired through horizontal gene transfer (HGT) events. The dominance of Ascomycota fungi as the main eukaryotes in crustal fluids and the evidence for HGT point to these fungi as the putative hosts, making these the first putative fungi-Nucleocytoviricota specific association. Our study suggests active host-viral dynamics for the only eukaryotic group found in the subsurface oceanic crust and raises important questions about the impact of viral infection on the productivity and biogeochemical cycling in this ecosystem.
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Aylward, Frank O., Jonatas S. Abrahão, Corina P. D. Brussaard, Matthias G. Fischer, Mohammad Moniruzzaman, Hiroyuki Ogata, and Curtis A. Suttle. "Taxonomic update for giant viruses in the order Imitervirales (phylum Nucleocytoviricota)." Archives of Virology 168, no. 11 (October 31, 2023). http://dx.doi.org/10.1007/s00705-023-05906-3.
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Ha, Anh D., Mohammad Moniruzzaman, and Frank O. Aylward. "Assessing the biogeography of marine giant viruses in four oceanic transects." ISME Communications 3, no. 1 (April 29, 2023). http://dx.doi.org/10.1038/s43705-023-00252-6.
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AbstractViruses of the phylum Nucleocytoviricota are ubiquitous in ocean waters and play important roles in shaping the dynamics of marine ecosystems. In this study, we leveraged the bioGEOTRACES metagenomic dataset collected across the Atlantic and Pacific Oceans to investigate the biogeography of these viruses in marine environments. We identified 330 viral genomes, including 212 in the order Imitervirales and 54 in the order Algavirales. We found that most viruses appeared to be prevalent in shallow waters (<150 m), and that viruses of the Mesomimiviridae (Imitervirales) and Prasinoviridae (Algavirales) are by far the most abundant and diverse groups in our survey. Five mesomimiviruses and one prasinovirus are particularly widespread in oligotrophic waters; annotation of these genomes revealed common stress response systems, photosynthesis-associated genes, and oxidative stress modulation genes that may be key to their broad distribution in the pelagic ocean. We identified a latitudinal pattern in viral diversity in one cruise that traversed the North and South Atlantic Ocean, with viral diversity peaking at high latitudes of the northern hemisphere. Community analyses revealed three distinct Nucleocytoviricota communities across latitudes, categorized by latitudinal distance towards the equator. Our results contribute to the understanding of the biogeography of these viruses in marine systems.
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Sheikh, Shaghayegh, Tomáš Pánek, Ondřej Gahura, Jiří Týč, Kristína Záhonová, Julius Lukeš, Marek Eliáš, and Hassan Hashimi. "A novel group of dynamin-related proteins shared by eukaryotes and giant viruses is able to remodel mitochondria from within the matrix." Molecular Biology and Evolution, June 6, 2023. http://dx.doi.org/10.1093/molbev/msad134.
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Abstract The diverse GTPases of the dynamin superfamily play various roles in the cell, as exemplified by the dynamin-related proteins (DRPs) Mgm1 and Opa1, which remodel the mitochondrial inner membrane in fungi and metazoans, respectively. Via an exhaustive search of genomic and metagenomic databases we found previously unknown DRP types occurring in diverse eukaryotes and giant viruses (phylum Nucleocytoviricota). One novel DRP clade, termed MidX, combined hitherto uncharacterized proteins from giant viruses and six distantly related eukaryote taxa (Stramenopiles, Telonemia, Picozoa, Amoebozoa, Apusomonadida, and Choanoflagellata). MidX stood out because it was not only predicted to be mitochondria-targeted, but also to assume a tertiary structure not observed in other DRPs before. To understand how MidX affects mitochondria, we exogenously expressed MidX from Hyperionvirus in the kinetoplastid Trypanosoma brucei, which lacks Mgm1 or Opa1 orthologs. MidX massively affected mitochondrial morphology from inside the matrix, where it closely associates with the inner membrane. This unprecedented mode of action is contrasts to those of Mgm1 and Opa1, which mediate inner membrane remodeling in the intermembrane space. We speculate that MidX was acquired in Nucleocytoviricota evolution by horizontal gene transfer from eukaryotes and is used by giant viruses to remodel host mitochondria during infection. MidX’s unique structure may be an adaptation for reshaping mitochondria from the inside. Finally, Mgm1 forms a sister to MidX and not Opa1 in our phylogenetic analysis, throwing into question the long-presumed homology of these DRPs with similar roles in sister lineages.
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Ha, Anh D., and Frank O. Aylward. "Automated classification of giant virus genomes using a random forest model built on trademark protein families." npj Viruses 2, no. 1 (March 8, 2024). http://dx.doi.org/10.1038/s44298-024-00021-9.
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AbstractViruses of the phylum Nucleocytoviricota, often referred to as “giant viruses,” are prevalent in various environments around the globe and play significant roles in shaping eukaryotic diversity and activities in global ecosystems. Given the extensive phylogenetic diversity within this viral group and the highly complex composition of their genomes, taxonomic classification of giant viruses, particularly incomplete metagenome-assembled genomes (MAGs) can present a considerable challenge. Here we developed TIGTOG (Taxonomic Information of Giant viruses using Trademark Orthologous Groups), a machine learning-based approach to predict the taxonomic classification of novel giant virus MAGs based on profiles of protein family content. We applied a random forest algorithm to a training set of 1531 quality-checked, phylogenetically diverse Nucleocytoviricota genomes using pre-selected sets of giant virus orthologous groups (GVOGs). The classification models were predictive of viral taxonomic assignments with a cross-validation accuracy of 99.6% at the order level and 97.3% at the family level. We found that no individual GVOGs or genome features significantly influenced the algorithm’s performance or the models’ predictions, indicating that classification predictions were based on a comprehensive genomic signature, which reduced the necessity of a fixed set of marker genes for taxonomic assigning purposes. Our classification models were validated with an independent test set of 823 giant virus genomes with varied genomic completeness and taxonomy and demonstrated an accuracy of 98.6% and 95.9% at the order and family level, respectively. Our results indicate that protein family profiles can be used to accurately classify large DNA viruses at different taxonomic levels and provide a fast and accurate method for the classification of giant viruses. This approach could easily be adapted to other viral groups.
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Rigou, Sofia, Sébastien Santini, Chantal Abergel, Jean-Michel Claverie, and Matthieu Legendre. "Past and present giant viruses diversity explored through permafrost metagenomics." Nature Communications 13, no. 1 (October 7, 2022). http://dx.doi.org/10.1038/s41467-022-33633-x.
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AbstractGiant viruses are abundant in aquatic environments and ecologically important through the metabolic reprogramming of their hosts. Less is known about giant viruses from soil even though two of them, belonging to two different viral families, were reactivated from 30,000-y-old permafrost samples. This suggests an untapped diversity of Nucleocytoviricota in this environment. Through permafrost metagenomics we reveal a unique diversity pattern and a high heterogeneity in the abundance of giant viruses, representing up to 12% of the sum of sequence coverage in one sample. Pithoviridae and Orpheoviridae-like viruses were the most important contributors. A complete 1.6 Mb Pithoviridae-like circular genome was also assembled from a 42,000-y-old sample. The annotation of the permafrost viral sequences revealed a patchwork of predicted functions amidst a larger reservoir of genes of unknown functions. Finally, the phylogenetic reconstructions not only revealed gene transfers between cells and viruses, but also between viruses from different families.
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Zhao, Zhennan, Youhua Huang, Congcong Liu, Dongjie Zhu, Shuaixin Gao, Sheng Liu, Ruchao Peng, et al. "Near-atomic architecture of Singapore grouper iridovirus and implications for giant virus assembly." Nature Communications 14, no. 1 (April 12, 2023). http://dx.doi.org/10.1038/s41467-023-37681-9.
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AbstractSingapore grouper iridovirus (SGIV), one of the nucleocytoviricota viruses (NCVs), is a highly pathogenic iridovirid. SGIV infection results in massive economic losses to the aquaculture industry and significantly threatens global biodiversity. In recent years, high morbidity and mortality in aquatic animals have been caused by iridovirid infections worldwide. Effective control and prevention strategies are urgently needed. Here, we present a near-atomic architecture of the SGIV capsid and identify eight types of capsid proteins. The viral inner membrane-integrated anchor protein colocalizes with the endoplasmic reticulum (ER), supporting the hypothesis that the biogenesis of the inner membrane is associated with the ER. Additionally, immunofluorescence assays indicate minor capsid proteins (mCPs) could form various building blocks with major capsid proteins (MCPs) before the formation of a viral factory (VF). These results expand our understanding of the capsid assembly of NCVs and provide more targets for vaccine and drug design to fight iridovirid infections.
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Pitot, Thomas M., Josephine Z. Rapp, Frederik Schulz, Catherine Girard, Simon Roux, and Alexander I. Culley. "Distinct and rich assemblages of giant viruses in Arctic and Antarctic lakes." ISME Communications, March 29, 2024. http://dx.doi.org/10.1093/ismeco/ycae048.
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Abstract Giant viruses (GVs) are key players in ecosystem functioning, biogeochemistry, and eukaryotic genome evolution. GV diversity and abundance in aquatic systems can exceed that of prokaryotes, but their diversity and ecology in lakes, especially polar ones, remains poorly understood. We conducted a comprehensive survey and meta-analysis of GV diversity across 20 lakes, spanning polar to temperate regions, combining our extensive lake metagenome database from the Canadian Arctic and subarctic with publicly available datasets. Leveraging a novel giant virus genome identification tool, we identified 3,304 GV metagenome-assembled genomes, revealing lakes as untapped GV reservoirs. Phylogenomic analysis highlighted their dispersion across all Nucleocytoviricota orders. Strong GV population endemism emerged between lakes from similar regions and biomes (Antarctic and Arctic), but a polar/temperate barrier in lacustrine GV populations and differences in their gene content could be observed. Our study establishes a robust genomic reference for future investigations into lacustrine GV ecology in fast changing polar environments.
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Homola, Miroslav, Carina R. Büttner, Tibor Füzik, Pavel Křepelka, Radka Holbová, Jiří Nováček, Marten L. Chaillet, et al. "Structure and replication cycle of a virus infecting climate-modulating alga Emiliania huxleyi." Science Advances 10, no. 15 (April 12, 2024). http://dx.doi.org/10.1126/sciadv.adk1954.
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The globally distributed marine alga Emiliania huxleyi has cooling effect on the Earth’s climate. The population density of E. huxleyi is restricted by Nucleocytoviricota viruses, including E. huxleyi virus 201 (EhV-201). Despite the impact of E. huxleyi viruses on the climate, there is limited information about their structure and replication. Here, we show that the dsDNA genome inside the EhV-201 virion is protected by an inner membrane, capsid, and outer membrane. EhV-201 virions infect E. huxleyi by using fivefold vertices to bind to and fuse the virus’ inner membrane with the cell plasma membrane. Progeny virions assemble in the cytoplasm at the surface of endoplasmic reticulum–derived membrane segments. Genome packaging initiates synchronously with the capsid assembly and completes through an aperture in the forming capsid. The genome-filled capsids acquire an outer membrane by budding into intracellular vesicles. EhV-201 infection induces a loss of surface protective layers from E. huxleyi cells, which enables the continuous release of virions by exocytosis.
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Queiroz, Victória Fulgêncio, Rodrigo Araújo Lima Rodrigues, Paulo Victor de Miranda Boratto, Bernard La Scola, Julien Andreani, and Jônatas Santos Abrahão. "Amoebae: Hiding in Plain Sight: Unappreciated Hosts for the Very Large Viruses." Annual Review of Virology 9, no. 1 (June 2, 2022). http://dx.doi.org/10.1146/annurev-virology-100520-125832.
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For decades, viruses have been isolated primarily from humans and other organisms. Interestingly, one of the most complex sides of the virosphere was discovered using free-living amoebae as hosts. The discovery of giant viruses in the early twenty-first century opened a new chapter in the field of virology. Giant viruses are included in the phylum Nucleocytoviricota and harbor large and complex DNA genomes (up to 2.7 Mb) encoding genes never before seen in the virosphere and presenting gigantic particles (up to 1.5 μm). Different amoebae have been used to isolate and characterize a plethora of new viruses with exciting details about novel viral biology. Through distinct isolation techniques and metagenomics, the diversity and complexity of giant viruses have astonished the scientific community. Here, we discuss the latest findings on amoeba viruses and how using these single-celled organisms as hosts has revealed entities that have remained hidden in plain sight for ages. Expected final online publication date for the Annual Review of Virology, Volume 9 is September 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Prodinger, Florian, Hisashi Endo, Yoshihito Takano, Yanze Li, Kento Tominaga, Tatsuhiro Isozaki, Romain Blanc-Mathieu, et al. "Year-round dynamics of amplicon sequence variant communities differ among eukaryotes, Imitervirales and prokaryotes in a coastal ecosystem." FEMS Microbiology Ecology 97, no. 12 (December 2021). http://dx.doi.org/10.1093/femsec/fiab167.
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ABSTRACT Coastal microbial communities are affected by seasonal environmental change, biotic interactions and fluctuating nutrient availability. We investigated the seasonal dynamics of communities of eukaryotes, a major group of double-stranded DNA viruses that infect eukaryotes (order Imitervirales; phylum Nucleocytoviricota), and prokaryotes in the Uranouchi Inlet, Kochi, Japan. We performed metabarcoding using ribosomal RNA genes and viral polB genes as markers in 43 seawater samples collected over 20 months. Eukaryotes, prokaryotes and Imitervirales communities characterized by the compositions of amplicon sequence variants (ASVs) showed synchronic seasonal cycles. However, the community dynamics showed intriguing differences in several aspects, such as the recovery rate after a year. We also showed that the differences in community dynamics were at least partially explained by differences in recurrence/persistence levels of individual ASVs among eukaryotes, prokaryotes and Imitervirales. Prokaryotic ASVs were the most persistent, followed by eukaryotic ASVs and Imitervirales ASVs, which were the least persistent. We argue that the differences in the specificity of interactions (virus–eukaryote vs prokaryote–eukaryote) as well as the niche breadth of community members were at the origin of the distinct community dynamics among eukaryotes, their viruses and prokaryotes.
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Farzad, Roxanna, Anh D. Ha, and Frank O. Aylward. "Diversity and genomics of giant viruses in the North Pacific Subtropical Gyre." Frontiers in Microbiology 13 (November 25, 2022). http://dx.doi.org/10.3389/fmicb.2022.1021923.
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Large double-stranded DNA viruses of the phylum Nucleocytoviricota, often referred to as “giant viruses,” are ubiquitous members of marine ecosystems that are important agents of mortality for eukaryotic plankton. Although giant viruses are known to be prevalent in marine systems, their activities in oligotrophic ocean waters remain unclear. Oligotrophic gyres constitute the majority of the ocean and assessing viral activities in these regions is therefore critical for understanding overall marine microbial processes. In this study, we generated 11 metagenome-assembled genomes (MAGs) of giant viruses from samples previously collected from Station ALOHA in the North Pacific Subtropical Gyre. Phylogenetic analyses revealed that they belong to the orders Imitervirales (n = 6), Algavirales (n = 4), and Pimascovirales (n = 1). Genome sizes ranged from ~119–574 kbp, and several of the genomes encoded predicted TCA cycle components, cytoskeletal proteins, collagen, rhodopsins, and proteins potentially involved in other cellular processes. Comparison with other marine metagenomes revealed that several have broad distribution across ocean basins and represent abundant viral constituents of pelagic surface waters. Our work sheds light on the diversity of giant viruses present in oligotrophic ocean waters across the globe.
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Zhao, Hongda, Ruixuan Zhang, Junyi Wu, Lingjie Meng, Yusuke Okazaki, Hiroyuki Hikida, and Hiroyuki Ogata. "A 1.5 Mb continuous endogenous viral region in the arbuscular mycorrhizal fungus Rhizophagus irregularis." Virus Evolution, October 31, 2023. http://dx.doi.org/10.1093/ve/vead064.
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Abstract Most fungal viruses are RNA viruses and no double-stranded DNA virus that infects fungi is known to date. A recent study detected DNA polymerase genes that originated from large dsDNA viruses in the genomes of basal fungi, suggestive of the existence of dsDNA viruses capable of infecting fungi. In this study, we searched for viral infection signatures in chromosome-level genome assemblies of the arbuscular mycorrhizal fungus Rhizophagus irregularis. We identified a continuous 1.5 Mb putative viral region on a chromosome in R. irregularis strain 4401. Phylogenetic analyses revealed that the viral region is related to viruses in the family Asfarviridae of the phylum Nucleocytoviricota. This viral region was absent in the genomes of four other R. irregularis strains and had fewer signals of fungal transposable elements than the other genomic regions, suggesting a recent and single insertion of a large dsDNA viral genome in the genome of this fungal strain. We also incidentally identified viral like sequences in genome assembly of the sea slug Elysia marginata that are evolutionally close to the 1.5 Mb putative viral region. In conclusion, our findings provide strong evidence of the recent infection of the fungus by a dsDNA virus.
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Arthofer, Patrick, Florian Panhölzl, Vincent Delafont, Alban Hay, Siegfried Reipert, Norbert Cyran, Stefanie Wienkoop, et al. "A giant virus infecting the amoeboflagellate Naegleria." Nature Communications 15, no. 1 (April 24, 2024). http://dx.doi.org/10.1038/s41467-024-47308-2.
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AbstractGiant viruses (Nucleocytoviricota) are significant lethality agents of various eukaryotic hosts. Although metagenomics indicates their ubiquitous distribution, available giant virus isolates are restricted to a very small number of protist and algal hosts. Here we report on the first viral isolate that replicates in the amoeboflagellate Naegleria. This genus comprises the notorious human pathogen Naegleria fowleri, the causative agent of the rare but fatal primary amoebic meningoencephalitis. We have elucidated the structure and infection cycle of this giant virus, Catovirus naegleriensis (a.k.a. Naegleriavirus, NiV), and show its unique adaptations to its Naegleria host using fluorescence in situ hybridization, electron microscopy, genomics, and proteomics. Naegleriavirus is only the fourth isolate of the highly diverse subfamily Klosneuvirinae, and like its relatives the NiV genome contains a large number of translation genes, but lacks transfer RNAs (tRNAs). NiV has acquired genes from its Naegleria host, which code for heat shock proteins and apoptosis inhibiting factors, presumably for host interactions. Notably, NiV infection was lethal to all Naegleria species tested, including the human pathogen N. fowleri. This study expands our experimental framework for investigating giant viruses and may help to better understand the basic biology of the human pathogen N. fowleri.
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Meng, Lingjie, Tom O. Delmont, Morgan Gaïa, Eric Pelletier, Antonio Fernàndez-Guerra, Samuel Chaffron, Russell Y. Neches, et al. "Genomic adaptation of giant viruses in polar oceans." Nature Communications 14, no. 1 (October 12, 2023). http://dx.doi.org/10.1038/s41467-023-41910-6.
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AbstractDespite being perennially frigid, polar oceans form an ecosystem hosting high and unique biodiversity. Various organisms show different adaptive strategies in this habitat, but how viruses adapt to this environment is largely unknown. Viruses of phyla Nucleocytoviricota and Mirusviricota are groups of eukaryote-infecting large and giant DNA viruses with genomes encoding a variety of functions. Here, by leveraging the Global Ocean Eukaryotic Viral database, we investigate the biogeography and functional repertoire of these viruses at a global scale. We first confirm the existence of an ecological barrier that clearly separates polar and nonpolar viral communities, and then demonstrate that temperature drives dramatic changes in the virus–host network at the polar–nonpolar boundary. Ancestral niche reconstruction suggests that adaptation of these viruses to polar conditions has occurred repeatedly over the course of evolution, with polar-adapted viruses in the modern ocean being scattered across their phylogeny. Numerous viral genes are specifically associated with polar adaptation, although most of their homologues are not identified as polar-adaptive genes in eukaryotes. These results suggest that giant viruses adapt to cold environments by changing their functional repertoire, and this viral evolutionary strategy is distinct from the polar adaptation strategy of their hosts.
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Matsuyama, Tomomasa, Ikunari Kiryu, Tohru Mekata, Tomokazu Takano, Kousuke Umeda, and Yuta Matsuura. "Pathogenicity, genomic analysis and structure of abalone asfa-like virus: evidence for classification in the family Asfarviridae." Journal of General Virology 104, no. 8 (August 2, 2023). http://dx.doi.org/10.1099/jgv.0.001875.
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This paper presents the rationale for classifying abalone asfa-like virus (AbALV) in the family Asfarviridae based on analyses of the host, whole genome and electron microscopic observations. AbALV caused >80 % cumulative mortality in an experimentally infected mollusc, Haliotis madaka. The AbALV genome was found to be linear, approximately 281 kb in length, with a G+C content of 31.32 %. Of the 309 predicted ORFs, 48 of the top hits with African swine fever virus (ASFV) genes in homology analysis were found to be in the central region of the genome. Synteny in the central region of the genome was conserved with ASFV. Similar to ASFV, paralogous genes were present at both ends of the genome. The pairwise average amino acid identity (AAI) between the AbALV and ASFV genomes was 33.97 %, within the range of intra-family AAI values for Nucleocytoviricota. Electron microscopy analysis of the gills revealed ~200 nm icosahedral virus particles in the cytoplasm of epithelial cells, and the size and morphology resembled ASFV. In addition to swine, ASFV also infects ticks, which are protostomes like abalone. The overall genome structure and virion morphology of AbALV and ASFV are similar, and both viruses infect protostomes, suggesting that AbALV is a new member of the family Asfarviridae.
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Arthofer, Patrick, Vincent Delafont, Anouk Willemsen, Florian Panhölzl, and Matthias Horn. "Defensive symbiosis against giant viruses in amoebae." Proceedings of the National Academy of Sciences 119, no. 36 (August 29, 2022). http://dx.doi.org/10.1073/pnas.2205856119.
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Protists are important regulators of microbial communities and key components in food webs with impact on nutrient cycling and ecosystem functioning. In turn, their activity is shaped by diverse intracellular parasites, including bacterial symbionts and viruses. Yet, bacteria–virus interactions within protists are poorly understood. Here, we studied the role of bacterial symbionts of free-living amoebae in the establishment of infections with nucleocytoplasmic large DNA viruses (Nucleocytoviricota). To investigate these interactions in a system that would also be relevant in nature, we first isolated and characterized a giant virus (Viennavirus, family Marseilleviridae) and a sympatric potential Acanthamoeba host infected with bacterial symbionts. Subsequently, coinfection experiments were carried out, using the fresh environmental isolates as well as additional amoeba laboratory strains. Employing fluorescence in situ hybridization and qPCR, we show that the bacterial symbiont, identified as Parachlamydia acanthamoebae , represses the replication of the sympatric Viennavirus in both recent environmental isolates as well as Acanthamoeba laboratory strains. In the presence of the symbiont, virions are still taken up, but viral factory maturation is inhibited, leading to survival of the amoeba host. The symbiont also suppressed the replication of the more complex Acanthamoeba polyphaga mimivirus and Tupanvirus deep ocean (Mimiviridae). Our work provides an example of an intracellular bacterial symbiont protecting a protist host against virus infections. The impact of virus–symbiont interactions on microbial population dynamics and eventually ecosystem processes requires further attention.
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Woo, Anthony C., Morgan Gaia, Julien Guglielmini, Violette Da Cunha, and Patrick Forterre. "Phylogeny of the Varidnaviria Morphogenesis Module: Congruence and Incongruence With the Tree of Life and Viral Taxonomy." Frontiers in Microbiology 12 (July 16, 2021). http://dx.doi.org/10.3389/fmicb.2021.704052.
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Double-stranded DNA viruses of the realm Varidnaviria (formerly PRD1-adenovirus lineage) are characterized by homologous major capsid proteins (MCPs) containing one (kingdom: Helvetiavirae) or two β-barrel domains (kingdom: Bamfordvirae) known as the jelly roll folds. Most of them also share homologous packaging ATPases (pATPases). Remarkably, Varidnaviria infect hosts from the three domains of life, suggesting that these viruses could be very ancient and share a common ancestor. Here, we analyzed the evolutionary history of Varidnaviria based on single and concatenated phylogenies of their MCPs and pATPases. We excluded Adenoviridae from our analysis as their MCPs and pATPases are too divergent. Sphaerolipoviridae, the only family in the kingdom Helvetiavirae, exhibit a complex history: their MCPs are very divergent from those of other Varidnaviria, as expected, but their pATPases groups them with Bamfordvirae. In single and concatenated trees, Bamfordvirae infecting archaea were grouped with those infecting bacteria, in contradiction with the cellular tree of life, whereas those infecting eukaryotes were organized into three monophyletic groups: the Nucleocytoviricota phylum, formerly known as the Nucleo-Cytoplasmic Large DNA Viruses (NCLDVs), Lavidaviridae (virophages) and Polintoviruses. Although our analysis mostly supports the recent classification proposed by the International Committee on Taxonomy of Viruses (ICTV), it also raises questions, such as the validity of the Adenoviridae and Helvetiavirae ranking. Based on our phylogeny, we discuss current hypotheses on the origin and evolution of Varidnaviria and suggest new ones to reconcile the viral and cellular trees.
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Akashi, Motohiro, Masaharu Takemura, and Seiichi Suzuki. "Continuous year-round isolation of giant viruses from brackish shoreline soils." Frontiers in Microbiology 15 (May 2, 2024). http://dx.doi.org/10.3389/fmicb.2024.1402690.
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Giant viruses, categorized under Nucleocytoviricota, are believed to exist ubiquitously in natural environments. However, comprehensive reports on isolated giant viruses remain scarce, with limited information available on unrecoverable strains, viral proliferation sites, and natural hosts. Previously, the author highlighted Pandoravirus hades, Pandoravirus persephone, and Mimivirus sp. styx, isolated from brackish water soil, as potential hotspots for giant virus multiplication. This study presents findings from nearly a year of monthly sampling within the same brackish water region after isolating the three aforementioned strains. This report details the recurrent isolation of a wide range of giant viruses. Each month, four soil samples were randomly collected from an approximately 5 × 10 m plot, comprising three soil samples and one water sample containing sediment from the riverbed. Acanthamoeba castellanii was used as a host for virus isolation. These efforts consistently yielded at least one viral species per month, culminating in a total of 55 giant virus isolates. The most frequently isolated species was Mimiviridae (24 isolates), followed by Marseilleviridae (23 isolates), Pandoravirus (6 isolates), and singular isolates of Pithovirus and Cedratvirus. Notably, viruses were not consistently isolated from any of the four samples every month, with certain sites yielding no viruses. Cluster analysis based on isolate numbers revealed that soil samples from May and water and sediment samples from January produced the highest number of viral strains. These findings underscore brackish coastal soil as a significant site for isolating numerous giant viruses, highlighting the non-uniform distribution along coastlines.
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Sun, Tsu-Wang, and Chuan Ku. "Unraveling Gene Content Variation Across Eukaryotic Giant Viruses Based on Network Analyses and Host Associations." Virus Evolution, September 16, 2021. http://dx.doi.org/10.1093/ve/veab081.
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Abstract The nucleocytoplasmic large DNA viruses (NCLDVs, phylum Nucleocytoviricota) infect vertebrates, invertebrates, algae, amoebae, and other unicellular organisms across supergroups of eukaryotes and in various ecosystems. The expanding collection of their genome sequences has revolutionized our view of virus genome size and coding capacity. Phylogenetic trees based on a few core genes are commonly used as a model to understand their evolution. However, the tree topology can differ between analyses and the vast majority of encoded genes might not share a common evolutionary history. To explore the whole-genome variation and evolution of NCLDVs, we dissected their gene contents using clustering, network, and comparative analyses. Our updated core-gene tree served as a framework to classify NCLDVs into families and intrafamilial lineages, but networks of individual genomes and family pangenomes showed patterns of gene sharing that contradict with the tree topology, in particular at higher taxonomic levels. Clustering of NCLDV genomes revealed variable granularity and degrees of gene sharing within each family, which cannot be inferred from the tree. At the level of NCLDV families, a correlation exists between gene content variation, but not core-gene sequence divergence, and host supergroup diversity. In addition, there is significantly higher gene sharing between divergent viruses that infect similar host types. The identified shared genes would be a useful resource for further functional analyses of NCLDV-host interactions. Overall this study provides a comprehensive view of gene repertoire variation in NCLDVs at different taxonomic levels, as well as a novel approach to studying the extremely diverse giant virus genomes.
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Perini, Laura, Katie Sipes, Athanasios Zervas, Christopher Bellas, Stefanie Lutz, Mohammad Moniruzzaman, Rey Mourot, Liane G. Benning, Martyn Tranter, and Alexandre M. Anesio. "Giant viral signatures on the Greenland ice sheet." Microbiome 12, no. 1 (May 17, 2024). http://dx.doi.org/10.1186/s40168-024-01796-y.
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Abstract Background Dark pigmented snow and glacier ice algae on glaciers and ice sheets contribute to accelerating melt. The biological controls on these algae, particularly the role of viruses, remain poorly understood. Giant viruses, classified under the nucleocytoplasmic large DNA viruses (NCLDV) supergroup (phylum Nucleocytoviricota), are diverse and globally distributed. NCLDVs are known to infect eukaryotic cells in marine and freshwater environments, providing a biological control on the algal population in these ecosystems. However, there is very limited information on the diversity and ecosystem function of NCLDVs in terrestrial icy habitats. Results In this study, we investigate for the first time giant viruses and their host connections on ice and snow habitats, such as cryoconite, dark ice, ice core, red and green snow, and genomic assemblies of five cultivated Chlorophyta snow algae. Giant virus marker genes were present in almost all samples; the highest abundances were recovered from red snow and the snow algae genomic assemblies, followed by green snow and dark ice. The variety of active algae and protists in these GrIS habitats containing NCLDV marker genes suggests that infection can occur on a range of eukaryotic hosts. Metagenomic data from red and green snow contained evidence of giant virus metagenome-assembled genomes from the orders Imitervirales, Asfuvirales, and Algavirales. Conclusion Our study highlights NCLDV family signatures in snow and ice samples from the Greenland ice sheet. Giant virus metagenome-assembled genomes (GVMAGs) were found in red snow samples, and related NCLDV marker genes were identified for the first time in snow algal culture genomic assemblies; implying a relationship between the NCLDVs and snow algae. Metatranscriptomic viral genes also aligned with metagenomic sequences, suggesting that NCLDVs are an active component of the microbial community and are potential “top-down” controls of the eukaryotic algal and protistan members. This study reveals the unprecedented presence of a diverse community of NCLDVs in a variety of glacial habitats dominated by algae.
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Machado, Talita B., Agnello C. R. Picorelli, Bruna L. de Azevedo, Isabella L. M. de Aquino, Victória F. Queiroz, Rodrigo A. L. Rodrigues, João Pessoa Araújo, et al. "Gene duplication as a major force driving the genome expansion in some giant viruses." Journal of Virology, November 21, 2023. http://dx.doi.org/10.1128/jvi.01309-23.
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ABSTRACT Giant viruses with their gigantic genomes are among the most intriguing components of the virosphere. How these viruses attained such giant genomes remains unclear, despite considerable efforts to understand this phenomenon. Here, we describe the discovery of cedratvirus pambiensis, an amoebal giant virus isolated in Brazil. Although the virion morphology and replication cycle of c. pambiensis are very similar to those described for other cedratviruses, whole genome sequencing revealed the largest cedratvirus genome ever described, with 623,564 base pairs and 842 predicted protein-coding genes (among them, 76 ORFans). Genome analysis has revealed an unprecedented number of paralogous genes, with ~73% of the c. pambiensis genome being composed of genes with two or more copies. Large families of functionally diverse paralogous genes included up to >70 copies and were distributed across the genome. The in-depth investigation of the mechanisms and origins of gene duplications revealed that both tandem-like duplications and distal transfer of syntenic blocks of genes contributed to the c. pambiensis genomic expansion. Finally, a comprehensive genome analysis of viruses from all known giant virus families suggested that gene duplication is one of the key mechanisms underlying genomic gigantism across the phylum Nucleocytoviricota . The expansion of viral genomes through successive duplications followed by subfunctionalization and exaptation of the paralogous gene copies may promote the adaptation of giant viruses to a variety of niches. IMPORTANCE Giant viruses are noteworthy not only due to their enormous particles but also because of their gigantic genomes. In this context, a fundamental question has persisted: how did these genomes evolve? Here we present the discovery of cedratvirus pambiensis, featuring the largest genome ever described for a cedratvirus. Our data suggest that the larger size of the genome can be attributed to an unprecedented number of duplicated genes. Further investigation of this phenomenon in other viruses has illuminated gene duplication as a key evolutionary mechanism driving genome expansion in diverse giant viruses. Although gene duplication has been described as a recurrent event in cellular organisms, our data highlights its potential as a pivotal event in the evolution of gigantic viral genomes.
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de Azevedo, Bruna Luiza, Victória Fulgêncio Queiroz, Isabella Luiza Martins de Aquino, Talita Bastos Machado, Felipe Lopes de Assis, Erik Reis, João Pessoa Araújo Júnior, et al. "The genomic and phylogenetic analysis of Marseillevirus cajuinensis raises questions about the evolution of Marseilleviridae lineages and their taxonomical organization." Journal of Virology, May 16, 2024. http://dx.doi.org/10.1128/jvi.00513-24.
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ABSTRACT Marseilleviruses (MsV) are a group of viruses that compose the Marseilleviridae family within the Nucleocytoviricota phylum. They have been found in different samples, mainly in freshwater. MsV are classically organized into five phylogenetic lineages (A/B/C/D/E), but the current taxonomy does not fully represent all the diversity of the MsV lineages. Here, we describe a novel strain isolated from a Brazilian saltwater sample named Marseillevirus cajuinensis. Based on genomics and phylogenetic analyses, M. cajuinensis exhibits a 380,653-bp genome that encodes 515 open reading frames. Additionally, M. cajuinensis encodes a transfer RNA, a feature that is rarely described for Marseilleviridae. Phylogeny suggests that M. cajuinensis forms a divergent branch within the MsV lineage A. Furthermore, our analysis suggests that the common ancestor for the five classical lineages of MsV diversified into three major groups. The organization of MsV into three main groups is reinforced by a comprehensive analysis of clusters of orthologous groups, sequence identities, and evolutionary distances considering several MsV isolates. Taken together, our results highlight the importance of discovering new viruses to expand the knowledge about known viruses that belong to the same lineages or families. This work proposes a new perspective on the Marseilleviridae lineages organization that could be helpful to a future update in the taxonomy of the Marseilleviridae family. IMPORTANCE Marseilleviridae is a family of viruses whose members were mostly isolated from freshwater samples. In this work, we describe the first Marseillevirus isolated from saltwater samples, which we called Marseillevirus cajuinensis . Most of M. cajuinensis genomic features are comparable to other Marseilleviridae members, such as its high number of unknown proteins. On the other hand, M. cajuinensis encodes a transfer RNA, which is a gene category involved in protein translation that is rarely described in this viral family. Additionally, our phylogenetic analyses suggested the existence of, at least, three major Marseilleviridae groups. These observations provide a new perspective on Marseilleviridae lineages organization, which will be valuable in future updates to the taxonomy of the family since the current official classification does not capture all the Marseilleviridae known diversity.
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Minch, Benjamin, Salma Akter, Alaina Weinheimer, M. Shaminur Rahman, Md Anowar Khasru Parvez, Sabita Rezwana Rahman, Md Firoz Ahmed, and Mohammad Moniruzzaman. "Phylogenetic diversity and functional potential of large and cell-associated viruses in the Bay of Bengal." mSphere, October 30, 2023. http://dx.doi.org/10.1128/msphere.00407-23.
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ABSTRACT The Bay of Bengal (BoB) is the world’s largest bay, offering essential services like fishing and recreation while holding significant economic value for coastal communities. However, the BoB faces environmental challenges from monsoons, freshwater inputs, rising sea levels, and intensified cyclones due to climate change. Human activities such as tourism and development also impact the region, necessitating a global change perspective. Despite its importance, microbial diversity and ecology in the BoB remain largely unexplored. We focused on large and cell-associated viruses (i.e., originating from the cellular size fraction), particularly giant viruses and large phages in two BoB coastal sites: Cox’s Bazar, a populated beach with freshwater influences, and Saint Martin Island, a less affected resort island. Metagenomic sequencing reveals a higher abundance and diversity of viruses in Cox’s Bazar and presence of viruses that suggest freshwater intrusion and runoff. We identified 1962 putative phage genomes (10–655 kbp). Notably, 16 “large” phages >100 kbp were found in Saint Martin, and a terminase large subunit marker gene phylogeny revealed substantial diversity of large phages along the BoB coast. The BoB virome encodes diverse functionalities, with a greater presence of auxiliary metabolic genes in the Cox’s Bazar viral community. Additionally, five giant virus genomes (phylum Nucleocytoviricota) encoding various functionalities are reconstructed from Cox’s Bazar (83–876 kbp). This pioneering study revealing the viral diversity and host interactions in coastal BoB lays the foundation for future investigations into viral impact on biogeochemical cycles and the microbial food web in this understudied environment. IMPORTANCE The BoB, the world’s largest bay, is of significant economic importance to surrounding countries, particularly Bangladesh, which heavily relies on its coastal resources. Concurrently, the BoB holds substantial ecological relevance due to the region’s high vulnerability to climate change-induced impacts. Yet, our understanding of the BoB’s microbiome in relation to marine food web and biogeochemical cycling remains limited. Particularly, there are little or no data on the viral diversity and host association in the BoB. We examined the viral community in two distinct BoB coastal regions to reveal a multitude of viral species interacting with a wide range of microbial hosts, some of which play key roles in coastal biogeochemical cycling or potential pathogens. Furthermore, we demonstrate that the BoB coast harbors a diverse community of large and giant viruses, underscoring the importance of investigating understudied environments to discover novel viral lineages with complex metabolic capacities.