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Commensalism in the Mimiviridae Giant Virus Family

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Commensalism in the Mimiviridae Giant Virus Family bioRxiv preprint doi: https://doi.org/10.1101/782383; this version posted September 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 1 Commensalism in the Mimiviridae giant virus family 2 3 Sandra Jeudya#*, Lionel Bertauxa#, Jean-Marie Alempica, Audrey Lartiguea, Matthieu Legendrea, Lucid 4 Belmudesb, Sébastien Santinia, Nadège Philippea, Laure Beucherb, Emanuele G. Biondic, Sissel Juuld, 5 Daniel J. Turnerd, Yohann Coutéb, Jean-Michel Claveriea*, Chantal Abergela* 6 aAix–Marseille Univ., Centre National de la Recherche Scientifique, Information Génomique & 7 Structurale, Unité Mixte de Recherche 7256 (Institut de Microbiologie de la Méditerranée, FR3479), 8 13288 Marseille Cedex 9, France 9 bUniv. Grenoble Alpes, CEA, INSERM, IRIG, BGE, 38000 Grenoble, France 10 cAix–Marseille Univ., Centre National de la Recherche Scientifique, Laboratoire de Chimie 11 Bactérienne, Unité Mixte de Recherche 7283 (Institut de Microbiologie de la Méditerranée, FR3479), 12 13009 Marseille, France 13 dOxford Nanopore Technologies Ltd, UK 14 #These authors contributed equally to the work 15 *Corresponding authors 16 Chantal Abergel, ORCID 0000-0003-1875-4049, [email protected], Phone: +33 491 17 825422 18 Jean-Michel Claverie, ORCID: 0000-0003-1424-0315, [email protected] 19 Sandra Jeudy, ORCID: 0000-0002-5297-0135, [email protected] 20 Short Title : Mimiviruses and their mobilomes 21 1 bioRxiv preprint doi: https://doi.org/10.1101/782383; this version posted September 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 22 Abstract 23 Acanthamoeba-infecting Mimiviridae belong to three clades: Mimiviruses (A), Moumouviruses (B) 24 and Megaviruses (C). The uniquely complex mobilome of these giant viruses includes virophages and 25 linear 7 kb-DNA molecules called “transpovirons”. We recently isolated a virophage (Zamilon vitis) 26 and two transpovirons (maBtv and mvCtv) respectively associated to B-clade and C-clade mimiviruses. 27 We used the capacity of the Zamilon virophage to replicate both on B-clade and C-clade host viruses 28 to investigate the three partite interaction network governing the propagation of transpovirons. We 29 found that the virophage could transfer both types of transpovirons to B-clade and C-clade host 30 viruses provided they were devoid of a resident transpoviron (permissive effect). If not, only the 31 resident transpoviron was replicated and propagated within the virophage progeny (dominance 32 effect). Although B- and C-clade viruses devoid of transpoviron could replicate both maBtv and mvCtv, 33 they did it with a lower efficiency across clades, suggesting an ongoing process of adaptive co- 34 evolution. We performed proteomic comparisons of host viruses and virophage particles carrying or 35 cleared of transpovirons in search of proteins involved in this adaptation process. These experiments 36 revealed that transpoviron-encoded proteins are synthetized during the combined 37 mimiviruses/virophage/transpoviron replication process and some of them are specifically 38 incorporated into the virophage and giant virus particles together with the cognate transpoviron 39 DNA. This study also highlights a unique example of intricate commensalism in the viral world, where 40 the transpoviron uses the virophage to propagate from one host virus to another and where the 41 Zamilon virophage and the transpoviron depend on their host giant virus to replicate, this without 42 affecting the giant virus infectious cycle, at least in laboratory conditions. 43 2 bioRxiv preprint doi: https://doi.org/10.1101/782383; this version posted September 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 44 Author Summary 45 The Mimiviridae are giant viruses with dsDNA genome up to 1.5 Mb. They build huge viral factories in 46 the host cytoplasm in which the nuclear-like virus-encoded functions (transcription and replication) 47 take place. They are themselves the target of infections by 20 kb-dsDNA virophages, replicating in 48 the giant virus factories. They can also be found associated with 7kb-DNA episomes, dubbed 49 transpovirons. We investigated the relationship between these three players by combining 50 competition experiments involving the newly isolated Zamilon vitis virophage as a vehicle for 51 transpovirons of different origins with proteomics analyses of virophage and giant virus particles. Our 52 results suggest that relationship of the virophage, the transpoviron, and their host giant virus, extend 53 the concept of commensalism to the viral world. 54 55 3 bioRxiv preprint doi: https://doi.org/10.1101/782383; this version posted September 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 56 Introduction 57 As of today, the Mimiviridae family appears composed of several distinct subfamilies (1–10) one 58 of which, the proposed Megamimivirinae (7,10,11), corresponds to the family members specifically 59 infecting Acanthamoeba (1,3–5,8). Members of this subfamilies, collectively refers to as 60 "mimiviruses" throughout this article, can be infected by dsDNA satellite viruses called virophages 61 only able to replicate using the already installed intracytoplasmic viral factory (6,12–15). These new 62 type of satellite viruses constitute the Lavidaviridae family (16). In addition to virophages, the 63 members of the mimiviruses can be found associated with a linear plasmid-like 7 kb-DNA called a 64 transpoviron (13,16,17) making their mobilome uniquely complex among the known large DNA virus 65 families. 66 Sputnik, the first discovered virophage, was found to infect the A-clade Mamavirus (12). Since it 67 caused the formation of abnormal, less infectious, MamavirusA particles, it was initially proposed that 68 virophages would in general protect host cells undergoing giant viruses’ infections. Such a protective 69 role was quantitatively demonstrated for the protozoan Cafeteria roenbergensis, infected by the 70 CroV (2)virus, in presence of the Mavirus virophage (18,19). However, it was later recognized that 71 some virophages replicated without visibly impairing the replication of their associated host virus. 72 This is the case for the mimiviruses of the B- or C-clades when infected by the Zamilon virophage 73 (15). On the other hand, members of the A-clade appeared non permissive to Zamilon replication 74 (15). The resistance to Zamilon infection was linked to a specific locus proposed to encode the viral 75 defence system MIMIVIRE (20–22) but the actual mechanisms governing the virulence of a given 76 virophage vis à vis its host virus remain to be elucidated (21,22). The rather ubiquitous transpovirons 77 might also be involved in the protection of the mimiviruses against the deleterious effects of 78 virophages infection. In this study we took advantage of a newly isolated virophage (Zamilon vitis) 79 and of its ability to propagate different transpovirons to investigate the specificity of the 80 transpoviron/host virus relationship. We also used B- and C-clades strains of mimiviruses originally 81 devoid of transpoviron to investigate the possible role of the transpoviron in the context of 4 bioRxiv preprint doi: https://doi.org/10.1101/782383; this version posted September 25, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. 82 virophage co-infections. Finally, we analyzed the proteome of virophage particles replicated on B- 83 and C-clades host viruses, with and without resident transpoviron, to identify transpoviron proteins 84 that could be involved in the co-evolution process allowing the transpovirons to be replicated by 85 mimiviruses. 86 87 Results 88 MegavirusC vitis, MoumouvirusB australiensis, MoumouvirusB maliensis and their 89 mobilomes 90 Three samples recovered from various locations (France, Australia and Mali) produced lytic 91 infections phenotypes when added to cultures of Acanthamoeba castellanii cells. Viral factories were 92 recognizable in the amoeba cells after DAPI staining and we observed the accumulation of spherical 93 particles visible by light microscopy in the culture medium (Fig. 1A). The corresponding virus 94 populations were cloned and amplified as previously described (23). In all cases, negative staining 95 electron microscopy (EM) images confirmed the presence of icosahedral virions of ~450 nm in 96 diameter with a stargate structure at one vertex, as was observed previously for all Mimiviridae 97 infecting Acanthamoeba cells (3,15,24,25). For some clones of the MegavirusC vitis giant virus, 98 associated icosahedral virions of ~70 nm diameter were also visible, suggesting the presence of 99 virophages (Fig. 1B-F). 100 Based on its genome sequence, this new isolate was determined to belong to the C-clade and named 101 MegavirusC vitis. Its associated virophage was named Zamilon vitis, in reference to its genomic 102 similarity with the original Zamilon virophage (15). In addition, the genome sequence assembly 103 process revealed the presence of a 7kb dsDNA sequence homologous to previously described 104 transpovirons (13). The MegavirusC vitis associated transpoviron was named mvCtv. The Australian 105 isolate was found to be a B-clade, and was named MoumouvirusB australiensis. It came with its own 106 transpoviron that we named maBtv.
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