Diversification of giant and large eukaryotic dsDNA viruses predated the origin of modern eukaryotes

Abstract

Giant and large eukaryotic double-stranded DNA viruses from the Nucleo-Cytoplasmic Large DNA Virus (NCLDV) assemblage represent a remarkably diverse and potentially ancient component of the eukaryotic virome. However, their origin(s), evolution, and potential roles in the emergence of modern eukaryotes remain subjects of intense debate. Here we present robust phylogenetic trees of NCLDVs, based on the 8 most conserved proteins responsible for virion morphogenesis and informational processes. Our results uncover the evolutionary relationships between different NCLDV families and support the existence of 2 superclades of NCLDVs, each encompassing several families. We present evidence strongly suggesting that the NCLDV core genes, which are involved in both informational processes and virion formation, were acquired vertically from a common ancestor. Among them, the largest subunits of the DNA-dependent RNA polymerase were transferred between 2 clades of NCLDVs and proto-eukaryotes, giving rise to 2 of the 3 eukaryotic DNA-dependent RNA polymerases. Our results strongly suggest that these transfers and the diversification of NCLDVs predated the emergence of modern eukaryotes, emphasizing the major role of viruses in the evolution of cellular domains.

Chloroviruses

“…The unusual nature of the virus-encoded glycosylation pathway led us to suggest that this glycan synthesis pathway might pre-date the evolution of the Golgi-ER glycosylation pathway [53,204]. The recent report that the evolutionary ancestor of giant viruses, including the chloroviruses, predated the origin of modern eukaryotes [215] is consistent with this suggestion.…”

Medusavirus Ancestor in a Proto-Eukaryotic Cell: Updating the Hypothesis for the Viral Origin of the Nucleus

“…Several features of giant viruses suggest the involvement of a viral ancestor in the process of eukaryotic cell evolution (Takemura et al, 2015;Guglielmini et al, 2019). NCLDVs can be divided into two major superclades, named MAPI, including the families Marseilleviridae, Ascoviridae, Pitholike viruses, and the family Iridoviridae, and PAM including the family Phycodnaviridae, Asfarviridae, Mimiviridae, and Pandoraviruses/Molliviruses (Guglielmini et al, 2019).…”

“…Several features of giant viruses suggest the involvement of a viral ancestor in the process of eukaryotic cell evolution (Takemura et al, 2015;Guglielmini et al, 2019). NCLDVs can be divided into two major superclades, named MAPI, including the families Marseilleviridae, Ascoviridae, Pitholike viruses, and the family Iridoviridae, and PAM including the family Phycodnaviridae, Asfarviridae, Mimiviridae, and Pandoraviruses/Molliviruses (Guglielmini et al, 2019). According to the molecular phylogenetic analysis of RNA polymerase genes, it has been hypothesized that the transfer of RNA polymerase genes between proto-eukaryotic cells and the PAM superclade, resulted in the evolution of 3 RNA polymerases in eukaryotes (Guglielmini et al, 2019).…”

“…NCLDVs can be divided into two major superclades, named MAPI, including the families Marseilleviridae, Ascoviridae, Pitholike viruses, and the family Iridoviridae, and PAM including the family Phycodnaviridae, Asfarviridae, Mimiviridae, and Pandoraviruses/Molliviruses (Guglielmini et al, 2019). According to the molecular phylogenetic analysis of RNA polymerase genes, it has been hypothesized that the transfer of RNA polymerase genes between proto-eukaryotic cells and the PAM superclade, resulted in the evolution of 3 RNA polymerases in eukaryotes (Guglielmini et al, 2019). Furthermore, the molecular phylogenetic analysis of DNA polymerase also suggested that gene transfer of DNA polymerase between protoeukaryotic cells and NCLDVs (Takemura et al, 2015).…”

“…Additionally, several proteins, such as bacteria-originated ancestral lamins described above, might have participated in the evolution of the eukaryotic nucleus structure. These evolutionary events, which links FECA to LECA, along with PAM evolution, and several lateral gene transfers, including DNA and RNA polymerases between cells and viruses, must have occurred, resulting in the diversification of NCLDVs (Takemura et al, 2015;Guglielmini et al, 2019). After the emergence of the nucleus, ancestral PAM infecting eukaryotic cells evolved and diversified to current viruses with several infection systems, such as the current medusavirus, pandoraviruses, and mollivirus, as well as Phycodnaviridae, Mimiviridae, and Asfarviridae families.…”