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

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 52865

Special Issue Editors


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Guest Editor
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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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
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Guest Editor
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

Published Papers (7 papers)

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Research

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14 pages, 1774 KiB  
Article
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 957
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 [...] Read more.
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
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17 pages, 6981 KiB  
Article
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
Viewed by 1126
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 [...] Read more.
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
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14 pages, 18475 KiB  
Article
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 1 | Viewed by 1217
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 [...] Read more.
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
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15 pages, 2270 KiB  
Article
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 1494
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 [...] Read more.
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
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16 pages, 2309 KiB  
Article
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 17 | Viewed by 42723
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, [...] Read more.
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
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Review

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11 pages, 680 KiB  
Review
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 2 | Viewed by 1741
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 [...] Read more.
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
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14 pages, 4682 KiB  
Review
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 1 | Viewed by 2150
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 [...] Read more.
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
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