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

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.

Discovery and Characterization of Novel RNA Viruses in Aquatic North American Wild Birds

“…For two viruses identified in black-back gulls and one from herring gulls, we obtained 537 nt and 396 nt sequences within the nsp3 region, respectively. These sequences were 99.5–100% identical to the B29 strain and only one synonymous substitution was found, indicating that the same virus circulates in both gull species, as previously reported for other viruses in the same populations [5].…”

“…Viral sequences identified with CACTUS, a Python-based wrapper script that handles PHRAP-based read assembly and BLASTn- and DIAMOND-based sequence taxonomy assignment, were used in this study as templates for primer design. To extend viral sequence information or obtain the complete viral genome, these primers were used to connect identified viral fragments by specific PCRs or to perform genome walking with the ViDiWa method as previously described [5], followed by Sanger sequencing. ViDiWa is a ViDiT-based nested-PCR method that uses tailed random octamers in combination with virus-specific primers to amplify unknown genomic regions flanking known sequences.…”

“…Isolated nucleic acids from a previous study [5] were used as templates for reverse transcription using SuperScript IV (Thermo Fisher Scientific, Waltham, MA, USA). Molecular screening was performed by hemi-nested PCRs with the primers listed in Table 1.…”

“…They have a global distribution and, thanks to their ability to fly long distances, are capable of migrating across biological and geographical borders and over broad spatial scales [1,3]. Because of these characteristics, birds play an important role in the dispersal of microbes and, therefore, influence microbial dynamics, impacting the ecology and evolution of various viruses and bacteria [3,4,5].…”

The characterization of two novel neotropical primate papillomaviruses supports the ancient within-species diversity model

“…2014 ; Gil da Costa et al. 2017 ; Canuti et al. 2019 ) and contributed to changing the paradigm ( Gottschling et al.…”