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Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie

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A special issue of Viruses (ISSN 1999-4915). This special issue belongs to the section "General Virology".

Deadline for manuscript submissions: closed (31 December 2023) | Viewed by 58661

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Special Issue Editors

Prof. Dr. David D. Dunigan

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Nebraska Center for Virology, University of Nebraska-Lincoln, Lincoln, NE 68583-0900, USA
Interests: virus; giant virus; chlorovirus; aquatic ecology; symbiosis; host–virus interactions; 5 great questions
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Dr. Juliana Reis Cortines

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Instituto de Microbiologia Paulo de Góes, Departamento de Virologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941-902, Brazil
Interests: giant viruses; NCLVD; virus cycle; virus structure; protein chemistry
Special Issues, Collections and Topics in MDPI journals

Prof. Dr. Rodrigo Araújo Lima Rodrigues

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Department of Microbiology, Federal University of Minas Gerais (UFMG), Belo Horizonte, Brazil
Interests: giant viruses; large viruses; viral genomics; virus evolution
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Prof. Jean-Michel Claverie has made seminal contributions to giant virus biology. His training and experience in biochemistry, particle physics and computer sciences helped him in his breakthrough discovery and characterizations of Mimivirus in 2003, kicking off the Era of Giant Viruses. He and his colleagues have now described four new families of giant viruses in exotic environments: Mega/Mimiviridae, the Pandoraviruses, Pithovirus and Mollivirus. The field of paleovirology is newly established, having emerged with the discovery of vital permafrost samples dating back 30,000 years. Although many of the discovered viruses have genes with no known homologs, Prof. Claverie and his team are providing visionary hypotheses of gene origin and evolution. At the root of these discoveries is his deep understanding of the field of bioinformatics, allowing for the exploration of the planet via multiomics and computational methods. Importantly, Prof. Claverie has disseminated his findings across the scientific community, sharing his knowledge and experiences with colleagues from around the world. We would like to celebrate Prof. Claverie’s significant achievements and intellectual insights with this Special Issue focused on giant viruses. Original reports and reviews on the research progress on giant viruses, as well as brief commentaries on Prof. Claverie’s influence on the field are welcome. We look forward to receiving your manuscripts.

Prof. Dr. David D. Dunigan
Prof. Dr. Juliana Reis Cortines
Prof. Dr. Rodrigo Araújo Lima Rodrigues
Guest Editors

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Keywords

giant virus
NCLDV
bioinformatics
mimivirus
paleovirology
genomics
virus hunter

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Published Papers (8 papers)

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14 pages, 1774 KiB

Open AccessArticle

Phaeoviruses Present in Cultured and Natural Kelp Species, Saccharina latissima and Laminaria hyperborea (Phaeophyceae, Laminariales), in Norway

by Eliana Ruiz Martínez, Dean A. Mckeown, Declan C. Schroeder, Gunnar Thuestad, Kjersti Sjøtun, Ruth-Anne Sandaa, Aud Larsen and Ingunn Alne Hoell

Viruses 2023, 15(12), 2331; https://doi.org/10.3390/v15122331 - 28 Nov 2023

Cited by 1 | Viewed by 1198

Abstract

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. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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Figure 1

Figure 1
Sampling stations. Full map to the left, and detailed sampling areas to the right. 1—Sognefjorden area, 2—Korsfjorden and Hardangerfjorden areas, and 3—Rogaland area. Full article ">Figure 2
Number of possible viral master variants per kelp sample and per location (A–C) or per area (D) on average. (A) L. hyperborea 2021–2022; (B) S. latissima 2021–2022; (C,D) S. latissima 2016–2018 (see <a href="#app1-viruses-15-02331" class="html-app">Table S3</a>). Full article ">Figure 3
Percentage of each possible viral master variant for both kelp species, year, and location (A–C), or per area (D), on average. (A) L. hyperborea 2021–2022; (B) S. latissima 2021–2022; (C,D) S. latissima 2016–2018. Full article ">Figure 4
Maximum likelihood phylogenetic tree of the amplified phaeoviral MCP fragment from our three viral master variant protein sequences (I, II, and III, magenta), aligned with other known giant viruses (Nucleocytoviricota) (see <a href="#app1-viruses-15-02331" class="html-app">Table S4</a> for accession numbers). Model of substitution: LG + G4. Nodes are bootstrap values (only bootstraps > 70 are shown), and branch lengths represent evolutionary distances. The tree is rooted with out-group Fowlpox virus. Full article ">Figure 5
Theoretical model for virus prevalence under 10 °C (blue line) or 20 °C (orange line) over time. Dashed lines represent the actual viral prevalence reduction due to viral genome segregation after meiosis for each temperature. Full article ">

17 pages, 6981 KiB

Open AccessArticle

Diversity, Relationship, and Distribution of Virophages and Large Algal Viruses in Global Ocean Viromes

by Zhenqi Wu, Ting Chu, Yijian Sheng, Yongxin Yu and Yongjie Wang

Viruses 2023, 15(7), 1582; https://doi.org/10.3390/v15071582 - 20 Jul 2023

Cited by 1 | Viewed by 1347

Abstract

Virophages are a group of small double-stranded DNA viruses that replicate and proliferate with the help of the viral factory of large host viruses. They are widely distributed in aquatic environments but are more abundant in freshwater ecosystems. Here, we mined the Global Ocean Viromes 2.0 (GOV 2.0) dataset for the diversity, distribution, and association of virophages and their potential host large viruses in marine environments. We identified 94 virophage sequences (>5 kbp in length), of which eight were complete genomes. The MCP phylogenetic tree showed that the GOV virophages were widely distributed on the global virophage tree but relatively clustered on three major branches. The gene-sharing network divided GOV virophages into 21 outliers, 2 overlaps, and 14 viral clusters, of which 4 consisted of only the GOV virophages. We also identified 45 large virus sequences, 8 of which were >100 kbp in length and possibly involved in cell–virus–virophage (C–V–v) trisome relationships. The potential eukaryotic hosts of these eight large viruses and the eight virophages with their complete genomes identified are likely to be algae, based on comparative genomic analysis. Both homologous gene and codon usage analyses support a possible interaction between a virophage (GOVv18) and a large algal virus (GOVLV1). These results indicate that diverse and novel virophages and large viruses are widespread in global marine environments, suggesting their important roles and the presence of complicated unknown C–V–v relationships in marine ecosystems. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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Figure 1
GOV virophage sequences identified. Full article ">Figure 2
The MCP phylogenetic tree of the GOV virophages. The GOV virophage sequences are marked in grey; blue, green, and orange dashed lines indicate the three major clades of GOV virophages. The colorful dots on the top of the branches are labeled for the sampling source of the sequences, and the colorful dots near the sequence names represent the taxonomic ranks of the sequences. DSLV, Dishui Lake virophage; OLV, Organic Lake virophage; RNV, Rio Negro virophage; YSLV, Yellowstone Lake virophage; QLV, Qinghai Lake virophage. Full article ">Figure 3
The gene-sharing network of the GOV virophages. (A) The GOV virophage sequences (>10 kb) are marked in purple, and the reference sequences (>10 kb) classified as Maveriviricetes in the IMG/VR v4 database are marked in grey. The VCs where the GOV virophages were grouped are indicated with black dashed lines and the Roman numerals. (B) The VCs in which the GOV virophages were clustered are shown in the magnification. The grey color represents the reference sequences in the IMG/VR database, the different colors represent the different VCs, and the triangles are marked for the GOV virophages. Full article ">Figure 4
Physical map of the complete genomes of eight GOV virophages. ORFs in different colors represent different functional categories. Inner zigzag grey line denotes GC content. The linear genome of GOVv6 is shown in open circle, and the black arrow points to the opening. Full article ">Figure 5
ViPTree of 45 GOV large viruses (incomplete genomic sequence > 5 kbp). The colors indicate the GOV large virus sequences. Blue indicates the Mimiviridae -related sequences, green indicates the Phycodnaviridae -related sequences, and orange indicates other large viruses. Sequences with a background color are those larger than 100 kb in length and the numbers represent sequences numbered in descending order according to their length. CVXW 01, Chlorella Virus XW01; CroV, Cafeteria roenbergensis virus; Moumouvirus, Acanthamoeba polyphaga moumouvirus; Mimivirus, Acanthamoeba polyphaga mimivirus; Mamavirus, Acanthamoeba castellanii mamavirus; AaV, Aureococcus anophagefferens virus; DSLLAV, Dishui Lake large alga virus; CeV, Chrysochromulina ericina virus; OLPV, Organic Lake phycodnavirus; CpV, Chrysochromulina parva virus; PgV, Phaeocystis globosa virus; AtCV, Acanthocystis turfacea chlorella virus; PBCV, Paramecium bursaria chlorella virus; YSLPV, Yellowstone Lake phycodnavirus; DSLPV, Dishui Lake phycodnavirus; MPV, Micromonas pusilla virus; OtV, Ostreococcus tauri virus. Full article ">Figure 6
Genomic physical map (partial) of the eight GOV large viruses (sequence longer than 100 kb). ORFs in different colors represent different taxonomic categories of BLASTp top hits. Their proportions are shown in the pie chart in the center. Inner zigzag grey line denotes GC content. The black triangle indicates the break site of the genomic sequences. Full article ">Figure 7
Phylogenetic tree of the genes shared between the GOV virophages and large viruses. Protein sequences were used for analysis. (A) GOVv34, GOVLV6-7, and other large viruses. (B) GOVv18, GOVLVs (1–3 and 8–9), and other virophages and large viruses. The GOV virophages are marked in green, and the GOV large viruses are marked in blue. Full names of viruses are consistent with those provided in the <a href="#viruses-15-01582-f005" class="html-fig">Figure 5</a> legend. Full article ">Figure 8
Codon usage frequencies and preferences of the GOV virophages and large viruses. Columns show codon usage frequency of each given genome, and rows represent different viruses. Full names of viruses are consistent with those provided in the <a href="#viruses-15-01582-f002" class="html-fig">Figure 2</a> and <a href="#viruses-15-01582-f005" class="html-fig">Figure 5</a> legends. Full article ">Figure 9
Global geographical distribution of the GOV virophages and large viruses. Blue dots represent virophages, orange dots represent large viruses, and green dots represent co-existence of virophages and large viruses. The size of the dots represents the number of total virophage and large virus sequences found at the sampling sites. The pie chart shows the percentage of the number of virophage and large virus sequences at the co-existing sampling sites. Full article ">

14 pages, 18475 KiB

Open AccessArticle

Viral DNA Accumulation Regulates Replication Efficiency of Chlorovirus OSy-NE5 in Two Closely Related Chlorella variabilis Strains

by Ahmed Esmael, Irina V. Agarkova, David D. Dunigan, You Zhou and James L. Van Etten

Viruses 2023, 15(6), 1341; https://doi.org/10.3390/v15061341 - 9 Jun 2023

Cited by 2 | Viewed by 1389

Abstract

Many chloroviruses replicate in Chlorella variabilis algal strains that are ex-endosymbionts isolated from the protozoan Paramecium bursaria, including the NC64A and Syngen 2-3 strains. We noticed that indigenous water samples produced a higher number of plaque-forming viruses on C. variabilis Syngen 2-3 lawns than on C. variabilis NC64A lawns. These observed differences led to the discovery of viruses that replicate exclusively in Syngen 2-3 cells, named Only Syngen (OSy) viruses. Here, we demonstrate that OSy viruses initiate infection in the restricted host NC64A by synthesizing some early virus gene products and that approximately 20% of the cells produce a small number of empty virus capsids. However, the infected cells did not produce infectious viruses because the cells were unable to replicate the viral genome. This is interesting because all previous attempts to isolate host cells resistant to chlorovirus infection were due to changes in the host receptor for the virus. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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Figure 1

Figure 1
Growth of NC64A cells (A) and Syngen cells (B) after infection with OSy-NE5 at low MOI (0.001 PFU/cell) and high MOI (10 PFU/cell). Uninfected cells served as a negative control. The growth was monitored for 15 days PI and is expressed as number of cells/mL. (C) Images of the untreated and OSy-NE5-treated algal cultures. Full article ">Figure 2
Initial OSy-NE5 infection inhibits subsequent PBCV-1 replication on NC64A and Syngen cells. The number of PBCV-1 plaques on NC64A lawns after 96 h (y-axis) following initial exposures to viruses (MOI = 10 PFU/cell) PBCV-1, OSy-NE5, or ATCV-1 on NC64A and Syngen cells followed by a second exposure to PBCV-1 (x-axis). Full article ">Figure 3
Accumulation of virus protein in both permissive and nonpermissive hosts. (A) Western blot analysis showing dynamics of OSy-NE5 protein accumulation isolated from uninfected (0) and OSy-NE5-infected NC64A cells at 20 min, 1, 3-, 6-, 12-, and 24 h PI and Syngen cells at 0, 20 min, 1, 3, and 6 hr PI. (B) Western blot analysis showing dynamics of PBCV-1 protein accumulation isolated from uninfected (0) and PBCV-1-infected NC64A and Syngen cells at 20 min, 1, 3, 6 h PI. The red arrows indicate the viruses’ major capsid proteins. Blots were probed using anti-PBCV-1 protein antibody. Equal loading of protein occurred for each sample. Full article ">Figure 4
Transmission electron micrographs of the infection process of C. variabilis Syngen 2-3 and C. variabilis NC64A cells by OSy-NE5. (A,B) Attachment and release of OSy-NE5 DNA into Syngen cells. (C,D) Attachment and release of OSy-NE5 DNA into NC64A cells. Symbols: cell wall, Cw, and virus particle, V. Scale bars, 100 nm. Full article ">Figure 5
Transmission electron micrographs of OSy-NE5-infected and uninfected C. variabilis Syngen 2-3. (A) uninfected Syngen 2-3 cell, (B–D) 1 h, 3 h, and 6, respectively, after infection with OSy-NE5. Mature virus particles were formed at 6 h PI in Syngen cells. Symbols: chloroplast, C, pyrenoid, P, nucleus, N, nucleolus, Nu, cell wall, Cw, virus assembly center, VC, and virus particles, V. Scale bars, 500 nm. Full article ">Figure 6
Transmission electron micrographs of OSyNE-5-infected and uninfected C. variabilis NC64A. (A) Uninfected NC64A cell (B–F) 1, 3, 6, 12, and 24 h, respectively, after infection with OSy-NE5. Empty OSy-NE5 capsids were formed after 24 h PI, as shown by red arrows. Symbols: chloroplast, C, pyrenoid, P, nucleus, N, nucleolus, Nu, cell wall, Cw, virus assembly center, VC, and virus particles, V. Scale bars, 600 nm. Full article ">Figure 7
Close-up view of OSy-NE5 infection process of Syngen cells and NC64A cells. The left panel shows a Syngen 2-3 cell at 6 h PI with OSy-NE5, while the right panel shows a NC64A cell at 24 h PI with OSy-NE5. The red arrows are virus particles at different stages of development. Magnified sections of these stages are shown in the bottom panels (A–D): (A) viral empty capsid; (B) presumed initiation of DNA packaging; (C) partially packaged (mature) virus; (D) fully packaged virus particle. Note that the capsids in the NC64A-infected cells are empty of viral DNA. Scale bars, 100 nm (left panel) and 500 nm (right panel). Full article ">Figure 8
DNA dynamics of OSy-NE5 in Syngen and NC64A cells. Total DNA concentrations in OSy-NE5-infected NC64A (A) and Syngen (D) cells. Specific gene replication of OSy-NE5 on NC64A and Syngen cells was monitored using qPCR analysis by measuring the kinetics of two genes at various times PI. Two OSy-NE5 genes, OS5_104L (B) and OS5_154L (C), and their corresponding homologs in PBCV-1 A208R (E) and A312L (F), respectively, were selected for this experiment. The results shown are the quantification of each gene copies/cell established using a standard curve. PBCV-1 served as a positive control that shows gene replication in both hosts. Full article ">

15 pages, 2270 KiB

Open AccessArticle

Early-Phase Drive to the Precursor Pool: Chloroviruses Dive into the Deep End of Nucleotide Metabolism

by David D. Dunigan, Irina V. Agarkova, Ahmed Esmael, Sophie Alvarez and James L. Van Etten

Viruses 2023, 15(4), 911; https://doi.org/10.3390/v15040911 - 31 Mar 2023

Viewed by 1672

Abstract

Viruses face many challenges on their road to successful replication, and they meet those challenges by reprogramming the intracellular environment. Two major issues challenging Paramecium bursaria chlorella virus 1 (PBCV-1, genus Chlorovirus, family Phycodnaviridae) at the level of DNA replication are (i) the host cell has a DNA G+C content of 66%, while the virus is 40%; and (ii) the initial quantity of DNA in the haploid host cell is approximately 50 fg, yet the virus will make approximately 350 fg of DNA within hours of infection to produce approximately 1000 virions per cell. Thus, the quality and quantity of DNA (and RNA) would seem to restrict replication efficiency, with the looming problem of viral DNA synthesis beginning in only 60–90 min. Our analysis includes (i) genomics and functional annotation to determine gene augmentation and complementation of the nucleotide biosynthesis pathway by the virus, (ii) transcriptional profiling of these genes, and (iii) metabolomics of nucleotide intermediates. The studies indicate that PBCV-1 reprograms the pyrimidine biosynthesis pathway to rebalance the intracellular nucleotide pools both qualitatively and quantitatively, prior to viral DNA amplification, and reflects the genomes of the progeny virus, providing a successful road to virus infection. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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16 pages, 2309 KiB

Open AccessArticle

An Update on Eukaryotic Viruses Revived from Ancient Permafrost

by Jean-Marie Alempic, Audrey Lartigue, Artemiy E. Goncharov, Guido Grosse, Jens Strauss, Alexey N. Tikhonov, Alexander N. Fedorov, Olivier Poirot, Matthieu Legendre, Sébastien Santini, Chantal Abergel and Jean-Michel Claverie

Viruses 2023, 15(2), 564; https://doi.org/10.3390/v15020564 - 18 Feb 2023

Cited by 19 | Viewed by 45827

Abstract

One quarter of the Northern hemisphere is underlain by permanently frozen ground, referred to as permafrost. Due to climate warming, irreversibly thawing permafrost is releasing organic matter frozen for up to a million years, most of which decomposes into carbon dioxide and methane, further enhancing the greenhouse effect. Part of this organic matter also consists of revived cellular microbes (prokaryotes, unicellular eukaryotes) as well as viruses that have remained dormant since prehistorical times. While the literature abounds on descriptions of the rich and diverse prokaryotic microbiomes found in permafrost, no additional report about “live” viruses have been published since the two original studies describing pithovirus (in 2014) and mollivirus (in 2015). This wrongly suggests that such occurrences are rare and that “zombie viruses” are not a public health threat. To restore an appreciation closer to reality, we report the preliminary characterizations of 13 new viruses isolated from seven different ancient Siberian permafrost samples, one from the Lena river and one from Kamchatka cryosol. As expected from the host specificity imposed by our protocol, these viruses belong to five different clades infecting Acanthamoeba spp. but not previously revived from permafrost: Pandoravirus, Cedratvirus, Megavirus, and Pacmanvirus, in addition to a new Pithovirus strain. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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Figure 1
Morphological features guiding the preliminary identification of newly isolated viruses (negative staining, TEM). (A) The large ovoid particle (1000 nm in length) of Pandoravirus yedoma (strain Y2) (sample #5 in <a href="#viruses-15-00564-t001" class="html-table">Table 1</a>) showing the apex ostiole (white arrowhead) and the thick tegument characteristic of the Pandoraviridae family. (B) A mixture of Pandoravirus mammoth (strain Yana14) oblate particles and of Megavirus mammoth (strain Yana14) icosahedral particles exhibiting a “stargate” (white starfish-like structure crowning a vertex, white arrowhead) as seen in sample #7 (<a href="#viruses-15-00564-t001" class="html-table">Table 1</a>). (C) The elongated particle of Cedratvirus lena (strain DY0) (1500 nm in length) exhibits two apex cork-like structures (white arrowheads) (sample #2, <a href="#viruses-15-00564-t001" class="html-table">Table 1</a>). (D) The elongated particle of Pithovirus mammoth (1800 nm in length) (sample #7, <a href="#viruses-15-00564-t001" class="html-table">Table 1</a>) exhibiting a single apex cork-like structure (white arrowhead). (E) The large (770 nm in diameter) “hairy” icosahedral particle of Megavirus mammoth (strain Yana14), showing the “stargate” (white arrowhead) characteristic of the Megavirinae subfamily (sample #7, <a href="#viruses-15-00564-t001" class="html-table">Table 1</a>). (F) The smaller icosahedral particle (200 nm in diameter) of Pacmanvirus lupus (strain Tums2) (sample #9, <a href="#viruses-15-00564-t001" class="html-table">Table 1</a>) typical of asfarviruses/pacmanviruses. Full article ">Figure 2
Maximum-likelihood phylogenetic relationships of the available Pandoravirus isolates. The tree (rooted at midpoint) was built using IQ-TREE (version 1.6.2) [<a href="#B54-viruses-15-00564" class="html-bibr">54</a>] from 2067 gap-free sites in the multiple alignment of 17 RNA polymerases (RPB1) protein (best fit model: “JTT + F + I + G4”). The permafrost isolates (in bold) are distributed between the two separate Pandoraviridae clades previously documented [<a href="#B55-viruses-15-00564" class="html-bibr">55</a>]. Accession numbers are indicated following the isolate name when available. Full article ">Figure 3
Maximum-likelihood phylogenetic relationships of the closest Pacmanvirus lupus relatives (using RPB1 homologs, <a href="#viruses-15-00564-t007" class="html-table">Table 7</a>). The tree (rooted at midpoint) was built using IQ-TREE (version 1.6.2) [<a href="#B54-viruses-15-00564" class="html-bibr">54</a>] (best fit model: “LG + F + I + G4”). The two closest Mimiviridae RPB1 sequences are used as an outgroup. The tree was built from 1314 gap-free sites in the multiple alignment of 9 RNA polymerases (RPB1) protein sequences. Although Pacmanvirus lupus is well clustered with other pacmanviruses, this clade (together with faustovirus) appears more as a sister group rather than bona fide members within the Asfarviridae (ASFV) family. Accession numbers are indicated following the isolate name when available. Full article ">

Review

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29 pages, 6154 KiB

Open AccessReview

Are Viruses Taxonomic Units? A Protein Domain and Loop-Centric Phylogenomic Assessment

by Gustavo Caetano-Anollés

Viruses 2024, 16(7), 1061; https://doi.org/10.3390/v16071061 - 30 Jun 2024

Viewed by 1044

Abstract

Virus taxonomy uses a Linnaean-like subsumption hierarchy to classify viruses into taxonomic units at species and higher rank levels. Virus species are considered monophyletic groups of mobile genetic elements (MGEs) often delimited by the phylogenetic analysis of aligned genomic or metagenomic sequences. Taxonomic units are assumed to be independent organizational, functional and evolutionary units that follow a ‘natural history’ rationale. Here, I use phylogenomic and other arguments to show that viruses are not self-standing genetically-driven systems acting as evolutionary units. Instead, they are crucial components of holobionts, which are units of biological organization that dynamically integrate the genetics, epigenetic, physiological and functional properties of their co-evolving members. Remarkably, phylogenomic analyses show that viruses share protein domains and loops with cells throughout history via massive processes of reticulate evolution, helping spread evolutionary innovations across a wider taxonomic spectrum. Thus, viruses are not merely MGEs or microbes. Instead, their genomes and proteomes conduct cellularly integrated processes akin to those cataloged by the GO Consortium. This prompts the generation of compositional hierarchies that replace the ‘is-a-kind-of’ by a ‘is-a-part-of’ logic to better describe the mereology of integrated cellular and viral makeup. My analysis demands a new paradigm that integrates virus taxonomy into a modern evolutionarily centered taxonomy of organisms. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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11 pages, 680 KiB

Open AccessReview

From Mimivirus to Mirusvirus: The Quest for Hidden Giants

by Morgan Gaïa and Patrick Forterre

Viruses 2023, 15(8), 1758; https://doi.org/10.3390/v15081758 - 17 Aug 2023

Cited by 3 | Viewed by 2043

Abstract

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. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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14 pages, 4682 KiB

Open AccessReview

Asfarviruses and Closely Related Giant Viruses

by Sihem Hannat, Bernard La Scola, Julien Andreani and Sarah Aherfi

Viruses 2023, 15(4), 1015; https://doi.org/10.3390/v15041015 - 20 Apr 2023

Cited by 2 | Viewed by 2431

Abstract

Acanthamoeba polyphaga mimivirus, so called because of its “mimicking microbe”, was discovered in 2003 and was the founding member of the first family of giant viruses isolated from amoeba. These giant viruses, present in various environments, have opened up a previously unexplored field of virology. Since 2003, many other giant viruses have been isolated, founding new families and taxonomical groups. These include a new giant virus which was isolated in 2015, the result of the first co-culture on Vermamoeba vermiformis. This new giant virus was named “Faustovirus”. Its closest known relative at that time was African Swine Fever Virus. Pacmanvirus and Kaumoebavirus were subsequently discovered, exhibiting phylogenetic clustering with the two previous viruses and forming a new group with a putative common ancestor. In this study, we aimed to summarise the main features of the members of this group of giant viruses, including Abalone Asfarvirus, African Swine Fever Virus, Faustovirus, Pacmanvirus, and Kaumoebavirus. Full article

(This article belongs to the Special Issue Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie)

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Figure 1

Figure 1
Genome synteny between Abalone Asfarvirus genome and the ASFV-BA71V genome. Schematic genome alignment obtained using the Mauve software [<a href="#B102-viruses-15-01015" class="html-bibr">102</a>]. The analysis was performed using the genome of Abalone Asfarvirus (LC637659.1), draft genome and ASFV strain BA71V (NC_001659.2). The blocks illustrated above the x axis are in the positive strand (forward sense), while blocks below the x axis are in the negative strand (reverse sense). The names of each virus are indicated below the sequence. The connected lines represent the relatively similar blocks between the genomes. Full article ">Figure 2
Phylogenetic tree based on the DNA polymerase homologs of Asfarviridae and relative viruses. ASFV contains 38 DNA polymerase sequences. Protein alignment was performed using Mafft software (v7.471) with standard parameters. The tree was built using IQ-TREE 1.6.12 with LG + F + I + G4 as best-fit model and 10,000 ultrafast bootstrap replication. Poxviridae sequences were used as an outgroup. Full article ">Figure 3
Mauve alignment genome of some Asfarviridae and other related viruses. Schematic genome alignment obtained using the Mauve software [<a href="#B102-viruses-15-01015" class="html-bibr">102</a>]. The analysis was performed using the genome of ASFV strain BA71V (NC_001659.2), Abalone Asfarvirus (LC637659.1), Faustovirus E12 (KJ614390.1), Pacmanvirus (LT706986.1) and Kaumoebavirus (KX552040.1). The blocks illustrated above the x axis are in the positive strand (forward sense), while blocks below the x axis are in the negative strand (reverse sense). Names of each virus are indicated below the sequence. The connected lines represent the relatively similar blocks between the genomes. Full article ">

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Research Progresses of Giant Viruses: A Themed Issue Dedicated to Professor Jean-Michel Claverie

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