New Insight Into Avian Papillomavirus Ecology and Evolution From Characterization of Novel Wild Bird Papillomaviruses.

Marta Canuti,Ashley N K Kroyer,Hannah J Munro,Davor Ojkic,Gregory J Robertson,Hugh G Whitney,Andrew S Lang,Sheena Roul

doi:10.3389/fmicb.2019.00701

Abstract

Viruses in the family Papillomaviridae have circular dsDNA genomes of approximately 5.7–8.6 kb that are packaged within non-enveloped, icosahedral capsids. The known papillomavirus (PV) representatives infect vertebrates, and there are currently more than 130 recognized PV species in more than 50 genera. We identified 12 novel avian papillomavirus (APV) types in wild birds that could represent five distinct species and two genera. Viruses were detected in paired oropharyngeal/cloacal swabs collected from six bird species, increasing the number of avian species known to harbor PVs by 40%. A new duck PV (DuPV-3) was found in mallard and American black duck (27.6% estimated prevalence) that was monophyletic with other known DuPVs. A single viral type was identified in Atlantic puffin (PuPV-1, 9.8% estimated prevalence), while a higher genetic diversity was found in other Charadriiformes. Specifically, three types [gull PV-1 (GuPV-1), -2, and -3] were identified in two gull species (estimated prevalence of 17% and 2.6% in American herring and great black-backed gull, respectively), and seven types [kittiwake PV-1 (KiPV-1) through -7] were found in black-legged kittiwake (81.3% estimated prevalence). Significantly higher DuPV-3 circulation was observed in spring compared to fall and in adults compared to juveniles. The studied host species’ tendencies to be in crowded environments likely affect infection rates and their migratory behaviors could explain the high viral diversity, illustrating how host behavior can influence viral ecology and distribution. For DuPV-3, GuPV-1, PuPV-1, and KiPV-2, we obtained the complete genomic sequences, which showed the same organization as other known APVs. Phylogenetic analyses showed evidence for virus–host co-divergence at the host taxonomic levels of family, order, and inter-order, but we also observed that host-specificity constraints are relaxed among highly related hosts as we found cross-species transmission within ducks and within gulls. Furthermore, the phylogeny of viruses infecting the Charadriiformes did not match the host phylogeny and gull viruses formed distinct monophyletic clades with kittiwake viruses, possibly reflecting past host-switching events. Considering the vast PV genotype diversity in other hosts and the large number of bird species, many more APVs likely remain to be discovered.

Highlights

Papillomaviruses (PVs) are small, non-enveloped, icosahedral viruses of vertebrates with a circular dsDNA genome of approximately 5.7–8.6 kb
Our genome-walking efforts allowed us to obtain the complete genomic sequences of four novel avian papillomavirus (APV), the puffin PV-1 (PuPV-1), the gull PV-1 (GuPV-1), the duck PV (DuPV)-3, and the kittiwake PV-2 (KiPV-2), which were identified in an Atlantic puffin, an American herring gull, a mallard and a black-legged kittiwake, respectively
Most viruses contained the regulatory TATA box (TATAWAW) within the E6 gene promoter and a polyadenylation site (ATTAAA or AATAAA) for the mRNAs of the late genes (O’Connor et al, 1995). Another short (2–50 nt) non-coding sequence was present in most viruses between the E2 and L2 open-reading frames (ORFs) and this contained in some cases (PaPV-1, PuPV-1, GuPV-1, and KiPV-2) the predicted polyadenylation site for the late mRNAs

Summary

Introduction

Papillomaviruses (PVs) are small, non-enveloped, icosahedral viruses of vertebrates with a circular dsDNA genome of approximately 5.7–8.6 kb. Most PVs are contained within the subfamily Firstpapillomavirinae and are associated with amniote hosts (reptiles, birds, and mammals), while the subfamily Secondpapillomavirinae contains a single viral species that has been identified in a fish (Van Doorslaer et al, 2018). Their genomes contain several open-reading frames (ORFs), all located on the same DNA strand, encoding the structural or late proteins (L1 and L2) and several nonstructural or early proteins (E1–E9), and a non-coding regulatory region known as the long control region (LCR). The genomic structure is similar across different species, the number of encoded E proteins is variable and only the core ORFs E1, E2, L2, and L1 are present in all PV genomes characterized to date (Rector and Van Ranst, 2013)

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