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.

Highlights

  • While for decades most of the focus was given to pathogenic viruses and viruses infecting parasites of human, animals and plants for obvious reasons, they are recognized as major players in the environment and are by far the most abundant entities in all biotopes including oceans, fresh water, soil [1,2,3,4,5] and are even found in association with multicellular organisms’ microbiotes [6,7,8]

  • This finding was confirmed by the immediate replacement of mvtv by matv proteins in virophage particles synthetized with MB. australiensis

  • It appears that neither of the two transpovirons remains stably associated with a host virus for which it was a first encounter, while a preference could emerge once a stable association has been established by co-evolution (i.e. MB. australiensis with matv, MC. vitis with mvtv)

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Summary

Introduction

While for decades most of the focus was given to pathogenic viruses and viruses infecting parasites of human, animals and plants for obvious reasons, they are recognized as major players in the environment and are by far the most abundant entities in all biotopes including oceans, fresh water, soil [1,2,3,4,5] and are even found in association with multicellular organisms’ microbiotes [6,7,8] They have received a lot of attention with the discovery of Mimivirus, the first giant virus with icosahedral capsids visible by light microscopy, enclosing a genome of 1.2 Mb and thousand genes [9, 10]. We analyzed the proteome of virophage particles replicated on B- and C-clades host viruses, with and without resident transpoviron, to identify transpoviron proteins that could be involved in the coevolution process allowing the transpovirons to be replicated by mimiviruses

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