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Unconventional Viruses
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Unconventional Viruses (Closed)

A topical collection in Viruses (ISSN 1999-4915). This collection belongs to the section "Viruses of Plants, Fungi and Protozoa".

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Editor

Prof. Dr. Jean-Michel Claverie

E-Mail Website
Collection Editor
Aix Marseille Univ, CNRS, IGS, Structural and Genomic Information Laboratory (UMR7256), Mediterranean Institute of Microbiology (FR3479), 163 Avenue de Luminy, F-13288 Marseille, France
Interests: giant viruses; virus origin and evolution; epistemology of microbiology
Special Issues, Collections and Topics in MDPI journals

Topical Collection Information

Dear Colleagues,

Since its very beginning, with the serendipitous discovery of the tobacco mosaic virus by Dmitri Ivanovsky in 1892, virology has mostly focused on those viruses responsible for (often dreadful) diseases of human, animals, or plants. Most of the research was then dedicated to the mechanisms of pathogenicity rather than to the physiology of the viruses as biological entities. One noticeable exception was the study of bacteriophages that led to the basic concepts of modern cellular biology and to many of today’s molecular biology tools. About fifteen years ago, a second wind of virology occurred with the discovery of the first giant viruses infecting amoeba, rapidly followed by that of an unexpected diversity of families associated with other protozoan and algal hosts. Through isolations or large-scale environmental metagenomic studies, a flurry of new viruses has since been uncovered that are considered unconventional due to their virion size and morphology, unusual gene contents, or exotic modes of replication. Beyond their unanticipated diversity, these “unconventional viruses” are challenging the established borders between the viral and cellular worlds as well as traditional views on the origin of life.

This Special Issue will gladly welcome articles pertaining to any of these unconventional viruses, from virophages to multipartite RNA and DNA viruses, huge phages, archaeal viruses, giant DNA viruses, as well as to the emerging concept of virus-encoded metabolism.

Prof. Dr. Jean-Michel Claverie
Collection Editor

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Keywords

  • unconventional viruses
  • giant DNA viruses
  • huge phages
  • archaeal viruses
  • virophages

Related Special Issue

Published Papers (8 papers)

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2020

20 pages, 1020 KiB  
Review
Host Range and Coding Potential of Eukaryotic Giant Viruses
by Tsu-Wang Sun, Chia-Ling Yang, Tzu-Tong Kao, Tzu-Haw Wang, Ming-Wei Lai and Chuan Ku
Viruses 2020, 12(11), 1337; https://doi.org/10.3390/v12111337 - 21 Nov 2020
Cited by 26 | Viewed by 6680
Abstract
Giant viruses are a group of eukaryotic double-stranded DNA viruses with large virion and genome size that challenged the traditional view of virus. Newly isolated strains and sequenced genomes in the last two decades have substantially advanced our knowledge of their host diversity, [...] Read more.
Giant viruses are a group of eukaryotic double-stranded DNA viruses with large virion and genome size that challenged the traditional view of virus. Newly isolated strains and sequenced genomes in the last two decades have substantially advanced our knowledge of their host diversity, gene functions, and evolutionary history. Giant viruses are now known to infect hosts from all major supergroups in the eukaryotic tree of life, which predominantly comprises microbial organisms. The seven well-recognized viral clades (taxonomic families) have drastically different host range. Mimiviridae and Phycodnaviridae, both with notable intrafamilial genome variation and high abundance in environmental samples, have members that infect the most diverse eukaryotic lineages. Laboratory experiments and comparative genomics have shed light on the unprecedented functional potential of giant viruses, encoding proteins for genetic information flow, energy metabolism, synthesis of biomolecules, membrane transport, and sensing that allow for sophisticated control of intracellular conditions and cell-environment interactions. Evolutionary genomics can illuminate how current and past hosts shape viral gene repertoires, although it becomes more obscure with divergent sequences and deep phylogenies. Continued works to characterize giant viruses from marine and other environments will further contribute to our understanding of their host range, coding potential, and virus-host coevolution. Full article
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17 pages, 2197 KiB  
Article
Comparative Analysis of the Circular and Highly Asymmetrical Marseilleviridae Genomes
by Léo Blanca, Eugène Christo-Foroux, Sofia Rigou and Matthieu Legendre
Viruses 2020, 12(11), 1270; https://doi.org/10.3390/v12111270 - 7 Nov 2020
Cited by 12 | Viewed by 3104
Abstract
Marseilleviridae members are large dsDNA viruses with icosahedral particles 250 nm in diameter infecting Acanthamoeba. Their 340 to 390 kb genomes encode 450 to 550 protein-coding genes. Since the discovery of marseillevirus (the prototype of the family) in 2009, several strains were [...] Read more.
Marseilleviridae members are large dsDNA viruses with icosahedral particles 250 nm in diameter infecting Acanthamoeba. Their 340 to 390 kb genomes encode 450 to 550 protein-coding genes. Since the discovery of marseillevirus (the prototype of the family) in 2009, several strains were isolated from various locations, among which 13 are now fully sequenced. This allows the organization of their genomes to be deciphered through comparative genomics. Here, we first experimentally demonstrate that the Marseilleviridae genomes are circular. We then acknowledge a strong bias in sequence conservation, revealing two distinct genomic regions. One gathers most Marseilleviridae paralogs and has undergone genomic rearrangements, while the other, enriched in core genes, exhibits the opposite pattern. Most of the genes whose protein products compose the viral particles are located in the conserved region. They are also strongly biased toward a late gene expression pattern. We finally discuss the potential advantages of Marseilleviridae having a circular genome, and the possible link between the biased distribution of their genes and the transcription as well as DNA replication mechanisms that remain to be characterized. Full article
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16 pages, 3829 KiB  
Article
Diversity of tRNA Clusters in the Chloroviruses
by Garry A. Duncan, David D. Dunigan and James L. Van Etten
Viruses 2020, 12(10), 1173; https://doi.org/10.3390/v12101173 - 16 Oct 2020
Cited by 2 | Viewed by 2339
Abstract
Viruses rely on their host’s translation machinery for the synthesis of their own proteins. Problems belie viral translation when the host has a codon usage bias (CUB) that is different from an infecting virus due to differences in the GC content between the [...] Read more.
Viruses rely on their host’s translation machinery for the synthesis of their own proteins. Problems belie viral translation when the host has a codon usage bias (CUB) that is different from an infecting virus due to differences in the GC content between the host and virus genomes. Here, we examine the hypothesis that chloroviruses adapted to host CUB by acquisition and selection of tRNAs that at least partially favor their own CUB. The genomes of 41 chloroviruses comprising three clades, each infecting a different algal host, have been sequenced, assembled and annotated. All 41 viruses not only encode tRNAs, but their tRNA genes are located in clusters. While differences were observed between clades and even within clades, seven tRNA genes were common to all three clades of chloroviruses, including the tRNAArg gene, which was found in all 41 chloroviruses. By comparing the codon usage of one chlorovirus algal host, in which the genome has been sequenced and annotated (67% GC content), to that of two of its viruses (40% GC content), we found that the viruses were able to at least partially overcome the host’s CUB by encoding tRNAs that recognize AU-rich codons. Evidence presented herein supports the hypothesis that a chlorovirus tRNA cluster was present in the most recent common ancestor (MRCA) prior to divergence into three clades. In addition, the MRCA encoded a putative isoleucine lysidine synthase (TilS) that remains in 39/41 chloroviruses examined herein, suggesting a strong evolutionary pressure to retain the gene. TilS alters the anticodon of tRNAMet that normally recognizes AUG to then recognize AUA, a codon for isoleucine. This is advantageous to the chloroviruses because the AUA codon is 12–13 times more common in the chloroviruses than their host, further helping the chloroviruses to overcome CUB. Among large DNA viruses infecting eukaryotes, the presence of tRNA genes and tRNA clusters appear to be most common in the Phycodnaviridae and, to a lesser extent, in the Mimiviridae. Full article
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12 pages, 1887 KiB  
Review
The Unconventional Viruses of Ichneumonid Parasitoid Wasps
by Anne-Nathalie Volkoff and Michel Cusson
Viruses 2020, 12(10), 1170; https://doi.org/10.3390/v12101170 - 15 Oct 2020
Cited by 7 | Viewed by 6563
Abstract
To ensure their own immature development as parasites, ichneumonid parasitoid wasps use endogenous viruses that they acquired through ancient events of viral genome integration. Thousands of species from the campoplegine and banchine wasp subfamilies rely, for their survival, on their association with these [...] Read more.
To ensure their own immature development as parasites, ichneumonid parasitoid wasps use endogenous viruses that they acquired through ancient events of viral genome integration. Thousands of species from the campoplegine and banchine wasp subfamilies rely, for their survival, on their association with these viruses, hijacked from a yet undetermined viral taxon. Here, we give an update of recent findings on the nature of the viral genes retained from the progenitor viruses and how they are organized in the wasp genome. Full article
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22 pages, 3322 KiB  
Article
A Survey of Mycoviral Infection in Fusarium spp. Isolated from Maize and Sorghum in Argentina Identifies the First Mycovirus from Fusarium verticillioides
by Andrés Gustavo Jacquat, Martín Gustavo Theumer, María Carmen Cañizares, Humberto Julio Debat, Juliana Iglesias, María Dolores García Pedrajas and José Sebastián Dambolena
Viruses 2020, 12(10), 1161; https://doi.org/10.3390/v12101161 - 14 Oct 2020
Cited by 13 | Viewed by 4336
Abstract
Mycoviruses appear to be widespread in Fusarium species worldwide. The aim of this work was to identify mycoviral infections in Fusarium spp., isolated from maize and sorghum grown in Argentina, and to estimate their potential effects on the pathogenicity and toxigenesis of the [...] Read more.
Mycoviruses appear to be widespread in Fusarium species worldwide. The aim of this work was to identify mycoviral infections in Fusarium spp., isolated from maize and sorghum grown in Argentina, and to estimate their potential effects on the pathogenicity and toxigenesis of the host fungus towards maize. Mycoviruses were identified in 2 out of 105 isolates analyzed; Fusarium verticillioides strain Sec505 and Fusarium andiyazi strain 162. They were characterized as members of the genus Mitovirus by high-throughput sequencing and sequence analysis. The F. verticillioides mitovirus was a novel mycovirus whereas the F. andiyazi mitovirus was found to be a new strain of a previously identified mitovirus. We have named these mitoviruses, Fusarium verticillioides mitovirus 1 (FvMV1) and Fusarium andiyazi mitovirus 1 strain 162 (FaMV1-162). To our knowledge, FvMV1 is the first mycovirus reported as naturally infecting F. verticillioides, the major causal agent of ear rot and fumonisin producer in corn. Both mitoviruses exhibited 100% vertical transmission rate to microconidia. The Fa162 strain infected with FaMV1-162 did not show phenotypic alterations. In contract, F. verticillioides Sec505 infected with FvMV1 showed increased virulence as well as microconidia and fumonisin-B1 production, compared with two uninfected strains. These results suggest that FvMV1 could have a role in modulating F. verticillioides pathogenicity and toxin production worth further exploring. Full article
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Graphical abstract

13 pages, 1158 KiB  
Opinion
Fundamental Difficulties Prevent the Reconstruction of the Deep Phylogeny of Viruses
by Jean-Michel Claverie
Viruses 2020, 12(10), 1130; https://doi.org/10.3390/v12101130 - 6 Oct 2020
Cited by 8 | Viewed by 3565
Abstract
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) [...] Read more.
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. Full article
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14 pages, 11992 KiB  
Article
A Functional K+ Channel from Tetraselmis Virus 1, a Member of the Mimiviridae
by Kerri Kukovetz, Brigitte Hertel, Christopher R. Schvarcz, Andrea Saponaro, Mirja Manthey, Ulrike Burk, Timo Greiner, Grieg F. Steward, James L. Van Etten, Anna Moroni, Gerhard Thiel and Oliver Rauh
Viruses 2020, 12(10), 1107; https://doi.org/10.3390/v12101107 - 29 Sep 2020
Cited by 3 | Viewed by 4179
Abstract
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 [...] Read more.
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. Full article
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18 pages, 2210 KiB  
Article
An Unconventional Flavivirus and Other RNA Viruses in the Sea Cucumber (Holothuroidea; Echinodermata) Virome
by Ian Hewson, Mitchell R. Johnson and Ian R. Tibbetts
Viruses 2020, 12(9), 1057; https://doi.org/10.3390/v12091057 - 22 Sep 2020
Cited by 13 | Viewed by 5058
Abstract
Sea cucumbers (Holothuroidea; Echinodermata) are ecologically significant constituents of benthic marine habitats. We surveilled RNA viruses inhabiting eight species (representing four families) of holothurian collected from four geographically distinct locations by viral metagenomics, including a single specimen of Apostichopus californicus affected by a [...] Read more.
Sea cucumbers (Holothuroidea; Echinodermata) are ecologically significant constituents of benthic marine habitats. We surveilled RNA viruses inhabiting eight species (representing four families) of holothurian collected from four geographically distinct locations by viral metagenomics, including a single specimen of Apostichopus californicus affected by a hitherto undocumented wasting disease. The RNA virome comprised genome fragments of both single-stranded positive sense and double stranded RNA viruses, including those assigned to the Picornavirales, Ghabrivirales, and Amarillovirales. We discovered an unconventional flavivirus genome fragment which was most similar to a shark virus. Ghabivirales-like genome fragments were most similar to fungal totiviruses in both genome architecture and homology and had likely infected mycobiome constituents. Picornavirales, which are commonly retrieved in host-associated viral metagenomes, were similar to invertebrate transcriptome-derived picorna-like viruses. The greatest number of viral genome fragments was recovered from the wasting A. californicus library compared to the asymptomatic A. californicus library. However, reads from the asymptomatic library recruited to nearly all recovered wasting genome fragments, suggesting that they were present but not well represented in the grossly normal specimen. These results expand the known host range of flaviviruses and suggest that fungi and their viruses may play a role in holothurian ecology. Full article
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