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Exploration of the propagation of transpovirons within Mimiviridae reveals a unique example of commensalism in the viral world.
ISME J. 2020 03; 14(3):727-739.IJ

Abstract

Acanthamoeba-infecting Mimiviridae are giant viruses with dsDNA genome up to 1.5 Mb. They build viral factories in the host cytoplasm in which the nuclear-like virus-encoded functions take place. They are themselves the target of infections by 20-kb-dsDNA virophages, replicating in the giant virus factories and can also be found associated with 7-kb-DNA episomes, dubbed transpovirons. Here we isolated a virophage (Zamilon vitis) and two transpovirons respectively associated to B- and C-clade mimiviruses. We found that the virophage could transfer each transpoviron provided the host viruses were devoid of a resident transpoviron (permissive effect). If not, only the resident transpoviron originally isolated from the corresponding virus was replicated and propagated within the virophage progeny (dominance effect). Although B- and C-clade viruses devoid of transpoviron could replicate each transpoviron, they did it with a lower efficiency across clades, suggesting an ongoing process of adaptive co-evolution. We analysed the proteomes of host viruses and virophage particles in search of proteins involved in this adaptation process. This study also highlights a unique example of intricate commensalism in the viral world, where the transpoviron uses the virophage to propagate and where the Zamilon virophage and the transpoviron depend on the giant virus to replicate, without affecting its infectious cycle.

Authors+Show Affiliations

Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France. Sandra.Jeudy@igs.cnrs-mrs.fr.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France.Université Grenoble Alpes, CEA, INSERM, IRIG, BGE, 38000, Grenoble, France.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France.Université Grenoble Alpes, CEA, INSERM, IRIG, BGE, 38000, Grenoble, France.Aix-Marseille Université, Centre National de la Recherche Scientifique, Laboratoire de Chimie Bactérienne, Unité Mixte de Recherche 7283; Institut de Microbiologie de la Méditerranée, FR3479, 13009, Marseille, France.Oxford Nanopore Technologies Ltd, Oxford Science Park, Oxford, UK.Oxford Nanopore Technologies Ltd, Oxford Science Park, Oxford, UK.Université Grenoble Alpes, CEA, INSERM, IRIG, BGE, 38000, Grenoble, France.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France. Jean-Michel.Claverie@univ-amu.fr.Aix-Marseille Université, Centre National de la Recherche Scientifique, Information Génomique & Structurale, Unité Mixte de Recherche 7256; Institut de Microbiologie de la Méditerranée, FR3479, 13288, Marseille, Cedex 9, France. Chantal.Abergel@igs.cnrs-mrs.fr.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

31822788

Citation

Jeudy, Sandra, et al. "Exploration of the Propagation of Transpovirons Within Mimiviridae Reveals a Unique Example of Commensalism in the Viral World." The ISME Journal, vol. 14, no. 3, 2020, pp. 727-739.
Jeudy S, Bertaux L, Alempic JM, et al. Exploration of the propagation of transpovirons within Mimiviridae reveals a unique example of commensalism in the viral world. ISME J. 2020;14(3):727-739.
Jeudy, S., Bertaux, L., Alempic, J. M., Lartigue, A., Legendre, M., Belmudes, L., Santini, S., Philippe, N., Beucher, L., Biondi, E. G., Juul, S., Turner, D. J., Couté, Y., Claverie, J. M., & Abergel, C. (2020). Exploration of the propagation of transpovirons within Mimiviridae reveals a unique example of commensalism in the viral world. The ISME Journal, 14(3), 727-739. https://doi.org/10.1038/s41396-019-0565-y
Jeudy S, et al. Exploration of the Propagation of Transpovirons Within Mimiviridae Reveals a Unique Example of Commensalism in the Viral World. ISME J. 2020;14(3):727-739. PubMed PMID: 31822788.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Exploration of the propagation of transpovirons within Mimiviridae reveals a unique example of commensalism in the viral world. AU - Jeudy,Sandra, AU - Bertaux,Lionel, AU - Alempic,Jean-Marie, AU - Lartigue,Audrey, AU - Legendre,Matthieu, AU - Belmudes,Lucid, AU - Santini,Sébastien, AU - Philippe,Nadège, AU - Beucher,Laure, AU - Biondi,Emanuele G, AU - Juul,Sissel, AU - Turner,Daniel J, AU - Couté,Yohann, AU - Claverie,Jean-Michel, AU - Abergel,Chantal, Y1 - 2019/12/10/ PY - 2019/09/09/received PY - 2019/11/28/accepted PY - 2019/11/27/revised PY - 2019/12/12/pubmed PY - 2020/7/1/medline PY - 2019/12/12/entrez SP - 727 EP - 739 JF - The ISME journal JO - ISME J VL - 14 IS - 3 N2 - Acanthamoeba-infecting Mimiviridae are giant viruses with dsDNA genome up to 1.5 Mb. They build viral factories in the host cytoplasm in which the nuclear-like virus-encoded functions take place. They are themselves the target of infections by 20-kb-dsDNA virophages, replicating in the giant virus factories and can also be found associated with 7-kb-DNA episomes, dubbed transpovirons. Here we isolated a virophage (Zamilon vitis) and two transpovirons respectively associated to B- and C-clade mimiviruses. We found that the virophage could transfer each transpoviron provided the host viruses were devoid of a resident transpoviron (permissive effect). If not, only the resident transpoviron originally isolated from the corresponding virus was replicated and propagated within the virophage progeny (dominance effect). Although B- and C-clade viruses devoid of transpoviron could replicate each transpoviron, they did it with a lower efficiency across clades, suggesting an ongoing process of adaptive co-evolution. We analysed the proteomes of host viruses and virophage particles in search of proteins involved in this adaptation process. This study also highlights a unique example of intricate commensalism in the viral world, where the transpoviron uses the virophage to propagate and where the Zamilon virophage and the transpoviron depend on the giant virus to replicate, without affecting its infectious cycle. SN - 1751-7370 UR - https://www.unboundmedicine.com/medline/citation/31822788/Exploration_of_the_propagation_of_transpovirons_within_Mimiviridae_reveals_a_unique_example_of_commensalism_in_the_viral_world_ L2 - https://doi.org/10.1038/s41396-019-0565-y DB - PRIME DP - Unbound Medicine ER -