Virology 130 Years After Ivanovsky—A Theme Issue Commemorating the Discovery of Viruses by Dmitri Ivanovsky

A special issue of Biomolecules (ISSN 2218-273X). This special issue belongs to the section "Biological Factors".

Deadline for manuscript submissions: closed (10 December 2022) | Viewed by 29285

Special Issue Editors


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Guest Editor
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA
Interests: molecular evolution; evolution of microbes and viruses; metagenomics; evolution of cancer; evolution of complexity; major transitions in evolution; origin of life

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Guest Editor
1. Institute of Protein Research, Russian Academy of Sciences, 142290 Pushchino, Russia
2. Institute of Theoretical and Experimental Biophysics, Russian Academy of Sciences, 142290 Pushchino, Russia
Interests: protein folding; bioinformatics and proteomics; aggregation; Alzheimer’s disease; intrinsically disordered proteins; antibacterial peptides
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Special Issue Information

Dear Colleagues,

Dmitry Ivanovsky made the first discovery of viruses in 1892. Although 130 years is not a traditional jubilee age, commemorating this discovery through a dedicated journal issue seems to be a must at a time when virology has become the area of science that is arguably of most immediate relevance to humanity.

For this Special Issue, we welcome primary research papers, conceptual articles,  and reviews on the scientific biography of Ivanovsky and the subsequent history of virus research; the definition and nature of viruses (e.g., are viruses life forms?); the current state of the art on Tobacco the Mosaic Virus, the virus discovered by Ivanovsky that became one of the classic models of virology and molecular biology; diversity, evolution, and origin of viruses; different approaches to virus classification and the current state of virus taxonomy;  ecology and biogeochemical roles of viruses; and other subjects in virus research that can be of interest to a broad audience of biologists.

We expect that this collection will become a timely overview of virus research, uniting its historical and contemporary aspects, which will educate biologists on the history and major concepts of virology and stimulate further research.

We look forward to receiving your contributions.

Dr. Eugene V. Koonin
Prof. Dr. Oxana V. Galzitskaya
Guest Editors

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Keywords

  • discovery of viruses
  • Dmitry Ivanovsky
  • definition of viruses
  • origin of viruses
  • evolution of viruses
  • virus taxonomy
  • main concepts of virology

Published Papers (10 papers)

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Research

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8 pages, 281 KiB  
Communication
Viriforms—A New Category of Classifiable Virus-Derived Genetic Elements
by Jens H. Kuhn and Eugene V. Koonin
Biomolecules 2023, 13(2), 289; https://doi.org/10.3390/biom13020289 - 03 Feb 2023
Cited by 3 | Viewed by 2848
Abstract
The International Committee on Taxonomy of Viruses (ICTV) recently accepted viriforms as a new polyphyletic category of classifiable virus-derived genetic elements, juxtaposed to the polyphyletic virus, viroid, and satellite nucleic acid categories. Viriforms are endogenized former viruses that have been exapted by their [...] Read more.
The International Committee on Taxonomy of Viruses (ICTV) recently accepted viriforms as a new polyphyletic category of classifiable virus-derived genetic elements, juxtaposed to the polyphyletic virus, viroid, and satellite nucleic acid categories. Viriforms are endogenized former viruses that have been exapted by their cellular hosts to fulfill functions important for the host’s life cycle. While morphologically resembling virions, particles made by viriforms do not package the viriform genomes but instead transport host genetic material. Known viriforms are highly diverse: members of family Polydnaviriformidae (former Polydnaviridae) have thus far been found exclusively in the genomes of braconid and ichneumonid parasitoid wasps, whereas the completely unrelated gene transfer agents (GTAs) are widely distributed among prokaryotes. In addition, recent discoveries likely extend viriforms to mammalian genomes. Here, we briefly outline the properties of these viriform groups and the first accepted and proposed ICTV frameworks for viriform classification. Full article
21 pages, 2060 KiB  
Article
Updated Virophage Taxonomy and Distinction from Polinton-like Viruses
by Simon Roux, Matthias G. Fischer, Thomas Hackl, Laura A. Katz, Frederik Schulz and Natalya Yutin
Biomolecules 2023, 13(2), 204; https://doi.org/10.3390/biom13020204 - 19 Jan 2023
Cited by 11 | Viewed by 4008
Abstract
Virophages are small dsDNA viruses that hijack the machinery of giant viruses during the co-infection of a protist (i.e., microeukaryotic) host and represent an exceptional case of “hyperparasitism” in the viral world. While only a handful of virophages have been isolated, a vast [...] Read more.
Virophages are small dsDNA viruses that hijack the machinery of giant viruses during the co-infection of a protist (i.e., microeukaryotic) host and represent an exceptional case of “hyperparasitism” in the viral world. While only a handful of virophages have been isolated, a vast diversity of virophage-like sequences have been uncovered from diverse metagenomes. Their wide ecological distribution, idiosyncratic infection and replication strategy, ability to integrate into protist and giant virus genomes and potential role in antiviral defense have made virophages a topic of broad interest. However, one limitation for further studies is the lack of clarity regarding the nomenclature and taxonomy of this group of viruses. Specifically, virophages have been linked in the literature to other “virophage-like” mobile genetic elements and viruses, including polinton-like viruses (PLVs), but there are no formal demarcation criteria and proper nomenclature for either group, i.e., virophage or PLVs. Here, as part of the ICTV Virophage Study Group, we leverage a large set of genomes gathered from published datasets as well as newly generated protist genomes to propose delineation criteria and classification methods at multiple taxonomic ranks for virophages ‘sensu stricto’, i.e., genomes related to the prototype isolates Sputnik and mavirus. Based on a combination of comparative genomics and phylogenetic analyses, we show that this group of virophages forms a cohesive taxon that we propose to establish at the class level and suggest a subdivision into four orders and seven families with distinctive ecogenomic features. Finally, to illustrate how the proposed delineation criteria and classification method would be used, we apply these to two recently published datasets, which we show include both virophages and other virophage-related elements. Overall, we see this proposed classification as a necessary first step to provide a robust taxonomic framework in this area of the virosphere, which will need to be expanded in the future to cover other virophage-related viruses such as PLVs. Full article
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18 pages, 1540 KiB  
Article
Methyltransferases of Riboviria
by Arcady Mushegian
Biomolecules 2022, 12(9), 1247; https://doi.org/10.3390/biom12091247 - 06 Sep 2022
Cited by 2 | Viewed by 1690
Abstract
Many viruses from the realm Riboviria infecting eukaryotic hosts encode protein domains with sequence similarity to S-adenosylmethionine-dependent methyltransferases. These protein domains are thought to be involved in methylation of the 5′-terminal cap structures in virus mRNAs. Some methyltransferase-like domains of Riboviria are homologous [...] Read more.
Many viruses from the realm Riboviria infecting eukaryotic hosts encode protein domains with sequence similarity to S-adenosylmethionine-dependent methyltransferases. These protein domains are thought to be involved in methylation of the 5′-terminal cap structures in virus mRNAs. Some methyltransferase-like domains of Riboviria are homologous to the widespread cellular FtsJ/RrmJ-like methyltransferases involved in modification of cellular RNAs; other methyltransferases, found in a subset of positive-strand RNA viruses, have been assigned to a separate “Sindbis-like” family; and coronavirus-specific Nsp13/14-like methyltransferases appeared to be different from both those classes. The representative structures of proteins from all three groups belong to a specific variety of the Rossmann fold with a seven-stranded β-sheet, but it was unclear whether this structural similarity extends to the level of conserved sequence signatures. Here I survey methyltransferases in Riboviria and derive a joint sequence alignment model that covers all groups of virus methyltransferases and subsumes the previously defined conserved sequence motifs. Analysis of the spatial structures indicates that two highly conserved residues, a lysine and an aspartate, frequently contact a water molecule, which is located in the enzyme active center next to the methyl group of S-adenosylmethionine cofactor and could play a key role in the catalytic mechanism of the enzyme. Phylogenetic evidence indicates a likely origin of all methyltransferases of Riboviria from cellular RrmJ-like enzymes and their rapid divergence with infrequent horizontal transfer between distantly related viruses. Full article
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11 pages, 3450 KiB  
Communication
Bioinformatic Analysis Predicts a Novel Genetic Module Related to Triple Gene and Binary Movement Blocks of Plant Viruses: Tetra-Cistron Movement Block
by Sergey Y. Morozov and Andrey G. Solovyev
Biomolecules 2022, 12(7), 861; https://doi.org/10.3390/biom12070861 - 21 Jun 2022
Cited by 3 | Viewed by 1577
Abstract
Previous studies have shown that the RNA genomes of some plant viruses encode two related genetic modules required for virus movement over the host body, containing two or three genes and named the binary movement block (BMB) and triple gene block (TGB), respectively. [...] Read more.
Previous studies have shown that the RNA genomes of some plant viruses encode two related genetic modules required for virus movement over the host body, containing two or three genes and named the binary movement block (BMB) and triple gene block (TGB), respectively. In this paper, we predict a novel putative-related movement gene module, called the tetra-cistron movement block (TCMB), in the virus-like transcriptome assemblies of the moss Dicranum scoparium and the Antarctic flowering plant Colobanthus quitensis. These TCMBs are encoded by smaller RNA components of putative two-component viruses related to plant benyviruses. Similar to the RNA2 of benyviruses, TCMB-containing RNAs have the 5′-terminal coat protein gene and include the RNA helicase gene which is followed by two small overlapping cistrons encoding hydrophobic proteins with a distant sequence similarity to the TGB2 and TGB3 proteins. Unlike TGB, TCMB also includes a fourth 5′-terminal gene preceding the helicase gene and coding for a protein showing a similarity to the double-stranded RNA-binding proteins of the DSRM AtDRB-like superfamily. Additionally, based on phylogenetic analysis, we suggest the involvement of replicative beny-like helicases in the evolution of the BMB and TCMB movement genetic modules. Full article
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Review

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0 pages, 1567 KiB  
Review
Endogenous Caulimovirids: Fossils, Zombies, and Living in Plant Genomes
by Héléna Vassilieff, Andrew D. W. Geering, Nathalie Choisne, Pierre-Yves Teycheney and Florian Maumus
Biomolecules 2023, 13(7), 1069; https://doi.org/10.3390/biom13071069 - 03 Jul 2023
Cited by 2 | Viewed by 1546
Abstract
The Caulimoviridae is a family of double-stranded DNA viruses that infect plants. The genomes of most vascular plants contain endogenous caulimovirids (ECVs), a class of repetitive DNA elements that is abundant in some plant genomes, resulting from the integration of viral DNA in [...] Read more.
The Caulimoviridae is a family of double-stranded DNA viruses that infect plants. The genomes of most vascular plants contain endogenous caulimovirids (ECVs), a class of repetitive DNA elements that is abundant in some plant genomes, resulting from the integration of viral DNA in the chromosomes of germline cells during episodes of infection that have sometimes occurred millions of years ago. In this review, we reflect on 25 years of research on ECVs that has shown that members of the Caulimoviridae have occupied an unprecedented range of ecological niches over time and shed light on their diversity and macroevolution. We highlight gaps in knowledge and prospects of future research fueled by increased access to plant genome sequence data and new tools for genome annotation for addressing the extent, impact, and role of ECVs on plant biology and the origin and evolutionary trajectories of the Caulimoviridae. Full article
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20 pages, 2777 KiB  
Review
Bacteriophages of the Order Crassvirales: What Do We Currently Know about This Keystone Component of the Human Gut Virome?
by Linda Smith, Ekaterina Goldobina, Bianca Govi and Andrey N. Shkoporov
Biomolecules 2023, 13(4), 584; https://doi.org/10.3390/biom13040584 - 24 Mar 2023
Cited by 6 | Viewed by 2640
Abstract
The order Crassvirales comprises dsDNA bacteriophages infecting bacteria in the phylum Bacteroidetes that are found in a variety of environments but are especially prevalent in the mammalian gut. This review summarises available information on the genomics, diversity, taxonomy, and ecology of this largely [...] Read more.
The order Crassvirales comprises dsDNA bacteriophages infecting bacteria in the phylum Bacteroidetes that are found in a variety of environments but are especially prevalent in the mammalian gut. This review summarises available information on the genomics, diversity, taxonomy, and ecology of this largely uncultured viral taxon. With experimental data available from a handful of cultured representatives, the review highlights key properties of virion morphology, infection, gene expression and replication processes, and phage-host dynamics. Full article
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37 pages, 2876 KiB  
Review
Cowpox Viruses: A Zoo Full of Viral Diversity and Lurking Threats
by Ryan C. Bruneau, Loubna Tazi and Stefan Rothenburg
Biomolecules 2023, 13(2), 325; https://doi.org/10.3390/biom13020325 - 08 Feb 2023
Cited by 4 | Viewed by 3095
Abstract
Cowpox viruses (CPXVs) exhibit the broadest known host range among the Poxviridae family and have caused lethal outbreaks in various zoo animals and pets across 12 Eurasian countries, as well as an increasing number of human cases. Herein, we review the history of [...] Read more.
Cowpox viruses (CPXVs) exhibit the broadest known host range among the Poxviridae family and have caused lethal outbreaks in various zoo animals and pets across 12 Eurasian countries, as well as an increasing number of human cases. Herein, we review the history of how the cowpox name has evolved since the 1700s up to modern times. Despite early documentation of the different properties of CPXV isolates, only modern genetic analyses and phylogenies have revealed the existence of multiple Orthopoxvirus species that are currently constrained under the CPXV designation. We further chronicle modern outbreaks in zoos, domesticated animals, and humans, and describe animal models of experimental CPXV infections and how these can help shaping CPXV species distinctions. We also describe the pathogenesis of modern CPXV infections in animals and humans, the geographic range of CPXVs, and discuss CPXV–host interactions at the molecular level and their effects on pathogenicity and host range. Finally, we discuss the potential threat of these viruses and the future of CPXV research to provide a comprehensive review of CPXVs. Full article
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9 pages, 749 KiB  
Review
From Contagium vivum fluidum to Riboviria: A Tobacco Mosaic Virus-Centric History of Virus Taxonomy
by F. Murilo Zerbini and Elliot W. Kitajima
Biomolecules 2022, 12(10), 1363; https://doi.org/10.3390/biom12101363 - 24 Sep 2022
Cited by 2 | Viewed by 3165
Abstract
Viruses were discovered as agents of disease in the late 19th century, but it was not until the 1930s that the nature of these agents was elucidated. Nevertheless, as soon as viral diseases started to be recognized and cataloged, there were attempts to [...] Read more.
Viruses were discovered as agents of disease in the late 19th century, but it was not until the 1930s that the nature of these agents was elucidated. Nevertheless, as soon as viral diseases started to be recognized and cataloged, there were attempts to classify and name viruses. Although these early attempts failed to be adopted by the nascent virology community, they are evidence of the human compulsion to try to organize the natural world into well-defined categories. Different classification schemes were proposed during the 20th century, but again none were widely embraced by virologists. In 1966, with the creation of the International Committee on Nomenclature of Viruses (eventually renamed as the International Committee on Taxonomy of Viruses), a more organized effort led to an official taxonomy in which viruses were classified into families and genera. At present, a much better understanding of the evolutionary relationships among viruses has led to the establishment of a 15-rank taxonomy based primarily on these evolutionary relationships. This review of virus taxonomy will be centered on the tobacco mosaic virus (TMV), the agent of the disease studied by Dmitry Ivanovsky and the first virus to be recognized as such, which was often historically at the center of major advancements in virology during the 20th century. Full article
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19 pages, 820 KiB  
Review
Viral Complexity
by Frank O. Aylward and Mohammad Moniruzzaman
Biomolecules 2022, 12(8), 1061; https://doi.org/10.3390/biom12081061 - 30 Jul 2022
Cited by 6 | Viewed by 4686
Abstract
Although traditionally viewed as streamlined and simple, discoveries over the last century have revealed that viruses can exhibit surprisingly complex physical structures, genomic organization, ecological interactions, and evolutionary histories. Viruses can have physical dimensions and genome lengths that exceed many cellular lineages, and [...] Read more.
Although traditionally viewed as streamlined and simple, discoveries over the last century have revealed that viruses can exhibit surprisingly complex physical structures, genomic organization, ecological interactions, and evolutionary histories. Viruses can have physical dimensions and genome lengths that exceed many cellular lineages, and their infection strategies can involve a remarkable level of physiological remodeling of their host cells. Virus–virus communication and widespread forms of hyperparasitism have been shown to be common in the virosphere, demonstrating that dynamic ecological interactions often shape their success. And the evolutionary histories of viruses are often fraught with complexities, with chimeric genomes including genes derived from numerous distinct sources or evolved de novo. Here we will discuss many aspects of this viral complexity, with particular emphasis on large DNA viruses, and provide an outlook for future research. Full article
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Other

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10 pages, 665 KiB  
Perspective
Opportunities and Challenges of Data-Driven Virus Discovery
by Chris Lauber and Stefan Seitz
Biomolecules 2022, 12(8), 1073; https://doi.org/10.3390/biom12081073 - 04 Aug 2022
Cited by 15 | Viewed by 2179
Abstract
Virus discovery has been fueled by new technologies ever since the first viruses were discovered at the end of the 19th century. Starting with mechanical devices that provided evidence for virus presence in sick hosts, virus discovery gradually transitioned into a sequence-based scientific [...] Read more.
Virus discovery has been fueled by new technologies ever since the first viruses were discovered at the end of the 19th century. Starting with mechanical devices that provided evidence for virus presence in sick hosts, virus discovery gradually transitioned into a sequence-based scientific discipline, which, nowadays, can characterize virus identity and explore viral diversity at an unprecedented resolution and depth. Sequencing technologies are now being used routinely and at ever-increasing scales, producing an avalanche of novel viral sequences found in a multitude of organisms and environments. In this perspective article, we argue that virus discovery has started to undergo another transformation prompted by the emergence of new approaches that are sequence data-centered and primarily computational, setting them apart from previous technology-driven innovations. The data-driven virus discovery approach is largely uncoupled from the collection and processing of biological samples, and exploits the availability of massive amounts of publicly and freely accessible data from sequencing archives. We discuss open challenges to be solved in order to unlock the full potential of data-driven virus discovery, and we highlight the benefits it can bring to classical (mostly molecular) virology and molecular biology in general. Full article
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