Abstract Papillomaviruses (PVs) are non-enveloped icosahedral viruses with a circular double-stranded DNA genome of ∼8,000 base pairs (bp). More than 200 different PV types have been identified to date in humans, which are distributed in five genera, with several strains associated with cancer development. Although widely distributed in vertebrates, Neotropical Primates (NP) PV infection was described for the first time only in 2016. Currently, four complete genomes of NP PVs have been characterized, three from Saimiri sciureus (SscPV1 to SscPV3) and one from Alouatta guariba (AgPV1). In this work, we describe two novel PV strains infecting Callithrix penicillata (provisionally named CpenPV1 and CpenPV2), using anal swab samples from animals residing at the Brasilia Primatology Center and next generation sequencing. The genomes of CpenPV1 (7,288 bp; 41.5% guanine-cytosine content - GC) and CpenPV2 (7,250 bp; 40.7% GC) contain the characteristic open reading frames (ORFs) for the early (E6, E7, E1, E2, and E4) and late (L2 and L1) PV genes. The L1 ORFs, commonly used for phylogenetic identification, share 76 per cent similarity with each other and differ 32 per cent from any other known PV, indicating that these new strains meet the criteria for defining novel species. PV genes phylogenetic variance was analyzed and different degrees of saturation revealed similar levels of topological heterogeneity, ruling out saturation as primary etiological factor for this phenomenon. Interestingly, the two CpenPV strains form a monophyletic clade within the Gammapapillomavirus genus (provisionally named gammapapillomavirus 32). Unlike for other NP PV strains, which grouped into a new sister genus of Alphapapillomavirus, this is the first report of NP PV strains grouping into a genus previously considered to exclusively comprise Old World Primates (OWP) PVs, including human PVs. These findings confirm the existence of a common ancestor for Gammapapillomavirus already infecting primates before the split of OWP and NP at ∼40 million years ago. Finally, our findings are consistent with an ancient within-species diversity model and emphasize the importance of increasing sampling to help understanding the PV-primate codivergence dynamics and pathogenic potential.

中文翻译：

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两种新型新热带灵长类乳头瘤病毒的特征支持古老的种内多样性模型

摘要 乳头瘤病毒 (PV) 是无包膜的二十面体病毒，具有约 8,000 个碱基对 (bp) 的环状双链 DNA 基因组。迄今为止，已在人类中鉴定出 200 多种不同的 PV 类型，它们分布在五个属中，其中一些菌株与癌症的发展有关。尽管在脊椎动物中广泛分布，但新热带灵长类动物 (NP) PV 感染仅在 2016 年才首次被描述。目前，已经表征了四个完整的 NP PV 基因组，三个来自 Saimiri sciureus（SscPV1 到 SscPV3）和一个来自 Alouatta guariba（ AgPV1)。在这项工作中，我们使用来自巴西利亚灵长类动物学中心的动物的肛门拭子样本和下一代测序来描述两种感染 Callithrix penicillata 的新型 PV 菌株（暂时命名为 CpenPV1 和 CpenPV2）。CpenPV1 (7, 288 bp；41.5% 鸟嘌呤胞嘧啶含量 - GC）和 CpenPV2（7,250 bp；40.7% GC）包含早期（E6、E7、E1、E2 和 E4）和晚期（L2 和 L1）的特征开放阅读框 (ORF)光伏基因。通常用于系统发育鉴定的 L1 ORF 彼此之间有 76% 的相似性，与任何其他已知 PV 的差异为 32%，表明这些新菌株符合定义新物种的标准。分析了 PV 基因的系统发育方差，不同程度的饱和度揭示了相似水平的拓扑异质性，排除了饱和度是这种现象的主要病因因素。有趣的是，这两个 CpenPV 毒株在 Gammapapillomavirus 属（暂时命名为 gammapapillomavirus 32）内形成了一个单系进化枝。与其他 NP PV 菌株不同，它被归入一个新的 Alphapapillomavirus 姐妹属，这是 NP PV 毒株归入一个以前被认为完全包含旧世界灵长类 (OWP) PVs 属的第一份报告，包括人类 PVs。这些发现证实了在大约 4000 万年前 OWP 和 NP 分裂之前已经感染灵长类动物的 Gammapapillomavirus 的共同祖先的存在。最后，我们的研究结果与古老的物种内多样性模型一致，并强调增加采样以帮助理解 PV-灵长类协同发散动力学和致病潜力的重要性。这些发现证实了在大约 4000 万年前 OWP 和 NP 分裂之前已经感染灵长类动物的 Gammapapillomavirus 的共同祖先的存在。最后，我们的发现与古老的物种内多样性模型一致，并强调增加采样以帮助理解 PV-灵长类协同发散动力学和致病潜力的重要性。这些发现证实了在大约 4000 万年前 OWP 和 NP 分裂之前已经感染灵长类动物的 Gammapapillomavirus 的共同祖先的存在。最后，我们的研究结果与古老的物种内多样性模型一致，并强调增加采样以帮助理解 PV-灵长类协同发散动力学和致病潜力的重要性。