The first complete papillomavirus genome characterized from a marsupial host: a novel isolate from Bettongia penicillata

Abstract

The first fully sequenced papillomavirus (PV) of marsupials, tentatively named Bettongia penicillata papillomavirus type 1 (BpPV1), was detected in papillomas from a woylie (Bettongia penicillata ogilbyi). The circular, double-stranded DNA genome contains 7,737 bp and encodes 7 open reading frames (ORFs), E6, E7, E1, E2, E4, L2, and L1, in typical PV conformation. BpPV1 is a close-to-root PV with L1 and L2 ORFs most similar to European hedgehog PV and bandicoot papillomatosis carcinomatosis virus types 1 and 2 (BPCV1 and -2). It appears that the BPCVs arose by recombination between an ancient PV and an ancient polyomavirus more than 10 million years ago.

FIG. 1.

Circular and linear genome maps of Bettongia penicillata papillomavirus type 1 (BpPV1), including a detail of the long control region, showing a putative origin of DNA replication (italics), predicted E2 binding sites (bold), and a predicted E1 binding site (underlined).

FIG. 2.

Neighbor-joining phylogenetic tree, based on a combined concatenated E1/E2/L2/L1 nucleotide sequence alignment of BpPV1 and 62 other PVs, using only the 1st and 2nd codon positions. The PV types were, in the genus Alphapapillomavirus, HPV32 (GenBank accession number NC_001586), HPV10 (NC_001576), HPV61 (NC_001694), HPV2a (NC_001352), HPV26 (NC_001583), HPV53 (NC_001593), HPV18 (NC_001357), HPV7 (NC_001595), HPV16 (NC_001526), HPV6 (NC_001355), HPV34 (NC_001587), rhesus PV type 1 (RhPV1; NC_001678), HPV54 (NC_001676), HPV90 (NC_004104), and HPV71 (AY330621); in the genus Betapapillomavirus, HPV5 (NC_001531), HPV9 (NC_001596), HPV49 (NC_001591), HPV92 (NC_004500), HPV96 (NC_005134), and Macaca fascicularis PV type 1 (MfPV1; EF028290); in the genus Gammapapillomavirus, HPV4 (NC_001457), HPV48 (NC_001690), HPV50 (NC_001691), and HPV60 (NC_001693); in the genus Deltapapillomavirus, European elk PV (EEPV; NC_001524), deer PV (DPV; NC_001523), ovine PV type 1 (OvPV1; NC_001789), and BPV1 (NC_001522); in the genus Epsilonpapillomavirus, BPV5 (NC_004195); in the genus Zetapapillomavirus, Equus caballus PV type 1 (EcPV1; NC_003748); in the genus Etapapillomavirus, Fringilla coelebs PV (FcPV; NC_004068); in the genus Thetapapillomavirus, Psittacus erithacus timnesh PV (PePV; NC_003973); in the genus Iotapapillomavirus, Mastomys natalensis PV (MnPV; NC_001605); in the genus Kappapapillomavirus, cottontail rabbit PV (CRPV; NC_001541) and rabbit oral PV (ROPV; NC_002232); in the genus Lambdapapillomavirus, COPV (NC_001619), Felis domesticus PV type 1 (FdPV1; NC_004765), and Procyon lotor PV type 1 (PlPV1; NC_007150); in the genus Mupapillomavirus, HPV1 (NC_001356); in the genus Nupapillomavirus, HPV41 (NC_001354); in the genus Xipapillomavirus, BPV3 (NC_004197); in the genus Omicronpapillomavirus, Phocoena spinipinnis PV type 1 (PsPV1; NC_003348); in the genus Pipapillomavirus, hamster oral PV (HaOPV; E15111); in the genus Rhopapillomavirus, Trichechus manatus latirostris PV type 1 (TmPV1; NC_006563); in the genus Sigmapapillomavirus, Erethizon dorsatum PV type 1 (EdPV1; NC_006951); and unclassified types Rousettus aegyptiacus PV type 1 (RaPV1; NC_008298), BPV7 (NC_007612), canine PV type 2 (CPV2; NC_006564), CPV3 (NC_008297), Capra hircus PV type 1 (ChPV1; NC_008032), Mastomys coucha PV type 2 (McPV2; DQ664501), Micromys minutus PV (MmPV; NC_008582), Ursus maritimus PV type 1 (UmPV1; NC_010739), Sus scrofa PV type 1a (SsPV1a; EF395818), Chelonia mydas PV type 1 (CmPV1; EU257705), Caretta caretta PV type 1 (CcaPV1; EU257704), Tursiops truncatus PV type 1 (TtPV1; NC_011109), TtPV2 (NC_008184), TtPV3 (NC_011110), and EHPV (NC_011765). The established PV genera are indicated by their Greek symbols. The scale bar indicates the genetic distance (in nucleotide substitutions per site), and the numbers at the internal nodes represent the bootstrap probability percentages as determined for 10,000 iterations by the neighbor-joining method. Only bootstrap values of 75% or more are shown.

FIG. 3.

Evolutionary relationship of the BpPV1 L1 and L2 sequences to BPCV1, BPCV2, and selected members of the Papillomaviridae. A neighbor-joining phylogenetic tree based on a concatenated alignment of the L1 and L2 sequences of BpPV1, BPCV2 (GenBank accession number NC_010817), BPCV1 (NC_010107), and 62 PVs (defined in the legend to Fig. 2). The established PV genera are indicated by their Greek symbols. The scale bar indicates the genetic distance (in nucleotide substitutions per site), and the numbers at the internal nodes represent the bootstrap probability percentages as determined for 10,000 iterations by the neighbor-joining method. Only bootstrap values of 75% or more are shown.