Exploration of the propagation of transpovirons within Mimiviridae reveals a unique example of commensalism in the viral world

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 Band 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 Band 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.

The DNA methylation landscape of giant viruses

“…We gathered PacBio SMRT data of diverse families from previously published genomes sequenced by our group to analyze the DNA methylation profile of a wide range of giant viruses. SMRT genomic data were collected for the following viruses: the Mimiviridae member moumouvirus australiensis and its associated transpoviron 28 , the Marseilleviridae member melbournevirus 37 and five pandoraviruses (pandoravirus celtis 38 , pandoravirus dulcis 30 , pandoravirus neocaledonia 30 , pandoravirus quercus 30 , and pandoravirus salinus 30 ). In addition, we resequenced on the PacBio platform the complete genomes of mollivirus sibericum, pithovirus sibericum, the Lavidaviridae member zamilon vitis and the megavirus vitis Mimiviridae member together with its associated transpoviron.…”

“…The first family of giant viruses to be discovered, the Mimiviridae, have megabase-sized AT-rich linear genomes packaged in icosahedral capsids [16][17][18] . Intriguingly some Mimiviridae members are infected by smaller 20-kb-dsDNA viruses, dubbed virophages 26,27 and sometimes found in association with 7-kb-DNA episomes called transpovirons 28,29 . In contrast to Mimiviridae, the pandoraviruses have GC-rich linear genomes, twice as big with up to 2.5 Mb, packaged in amphora-shaped capsids 22,30 .…”

“…Here, we use SMRT sequencing to survey the complete methylome of a large spectrum of giant viruses. We analyze two distinct Mimiviridae members and their associated transpovirons, as well as a virophage 28 . We also survey a Marseilleviridae member 37 , five distinct pandoraviruses 22,30,38 , a mollivirus 23 and a pithovirus 20 .…”

The DNA Methylation Landscape of Giant Viruses

“…Giant viruses of the Mimiviridae family are involved in complex network of interactions with the cellular host, the virophages, and the transpovirons (45,(87)(88)(89)(90). It has been proposed that R-M systems could be used as an anti-virophage agent in these multipartite systems (91).…”

“…Here we used SMRT sequencing to survey the complete methylome of a large spectrum of giant viruses. We analyzed two distinct Mimiviridae and their associated transpovirons as well as a virophage (45). We also surveyed a Marseilleviridae (46), five distinct Pandoraviruses (29,37,47), a Mollivirus (48) and a Pithovirus (26).…”