Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins

Abstract

The family Papillomaviridae contains more than 320 papillomavirus types, with most having been identified as infecting skin and mucosal epithelium in mammalian hosts. To date, only nine non-mammalian papillomaviruses have been described from birds (n = 5), a fish (n = 1), a snake (n = 1), and turtles (n = 2). The identification of papillomaviruses in sauropsids and a sparid fish suggests that early ancestors of papillomaviruses were already infecting the earliest Euteleostomi. The Euteleostomi clade includes more than 90 per cent of the living vertebrate species, and progeny virus could have been passed on to all members of this clade, inhabiting virtually every habitat on the planet. As part of this study, we isolated a novel papillomavirus from a 16-year-old female Adélie penguin (Pygoscelis adeliae) from Cape Crozier, Ross Island (Antarctica). The new papillomavirus shares ∼64 per cent genome-wide identity to a previously described Adélie penguin papillomavirus. Phylogenetic analyses show that the non-mammalian viruses (expect the python, Morelia spilota, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; Fulmarus glacialis), like the two turtle papillomaviruses, lacks a putative E9 protein that is found in all other avian papillomaviruses. Furthermore, the Northern fulmar papillomavirus has an E7 more similar to the mammalian viruses than the other avian papillomaviruses. Typical E6 proteins of mammalian papillomaviruses have two Zinc finger motifs, whereas the sauropsid papillomaviruses only have one such motif. Furthermore, this motif is absent in the fish papillomavirus. Thus, it is highly likely that the most recent common ancestor of the mammalian and sauropsid papillomaviruses had a single motif E6. It appears that a motif duplication resulted in mammalian papillomaviruses having a double Zinc finger motif in E6. We estimated the divergence time between Northern fulmar-associated papillomavirus and the other Sauropsid papillomaviruses be to around 250 million years ago, during the Paleozoic-Mesozoic transition and our analysis dates the root of the papillomavirus tree between 400 and 600 million years ago. Our analysis shows evidence for niche adaptation and that these non-mammalian viruses have highly divergent E6 and E7 proteins, providing insights into the evolution of the early viral (onco-)proteins.

Origin and evolution of papillomavirus (onco)genes and genomes

“…1). A recent study dated back this root to 481 Ma, albeit with a broad HPD interval (95% HPD 326 -656) (Van Doorslaer et al, 2017b). In our study, the root of the tree was dated back to 424 Ma (95% HPD: 402 -446) ( fig.…”

Prisoners of war — host adaptation and its constraints on virus evolution

“…For example, the phylogeny of spumaviruses closely follows that of their mammalian, amphibian and piscine hosts, consistent with virus-host co-speciation over 450 Myr 52,53 . The proposed co-evolution of papillomaviruses with their hosts suggests their similarly ancient origins of 400-600 Myr 54 . Increasingly divergent homologues of HBV have been observed as EVEs in birds and reptiles 50 , and exogenous hepadna-like viruses have recently been found in fish genomic libraries 55 .…”

Viruses associated with Antarctic wildlife: From serology based detection to identification of genomes using high throughput sequencing

“…Two novel papillomavirus, Pygoscelis adeliae papillomavirus 1, −2 (PaPV1, −2), was recently identified in Antarctica from feces and cloacal swab of Adélie penguins at Cape Crozier, Ross Island (Table 2, Fig. 1) using a HTS-informed approach (Van Doorslaer et al, 2017;Varsani et al, 2014). PaPV1 and −2 are related to other avian papillomaviruses, PaPV1 has been assigned to the genus Treisepsilonpapillomavirus whereas PaPV2 is currently unclassified and shares ∼64% genome-wide pairwise identity with PaPV1.…”