First New World Primate Papillomavirus Identification in the Atlantic Forest, Brazil:
            <i>Alouatta guariba papillomavirus 1</i>

Silvestre, Rodrigo Vellasco Duarte; Souza, Alex Júnior Souza de; Júnior, Edivaldo Costa Sousa; Silva, Allan Kaio; Mello, Wyller Alencar de; Nunes, Márcio Roberto Teixeira; Júnior, João Lídio da Silva Gonçalves Vianez; Cardoso, Jedson Ferreira; Vasconcelos, Janaína Mota de; Oliveira, Layanna Freitas de; Silva, Sandro Patroca da; Silva, Adriana Marques J. da; Fries, Brigida Gomes; Summa, Maria Eugênia Laurito; Sá, Lílian Rose Marques de

doi:10.1128/genomea.00725-16

Cited by 13 publications

(15 citation statements)

References 8 publications

(7 reference statements)

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“…We identified a contig that displays 95% identity to human papillomavirus 4, which might indicate an association with virus infections in these animals, similar to what has been described from howler capuchin monkeys (Alouatta fusca) [34]. However, lesions in the oral mucosae were not observed, and these viruses may thus be part of normal microbial content, as described previously for other species [35,36].…”

Section: Discussionsupporting

confidence: 82%

Viral diversity in oral cavity from Sapajus nigritus by metagenomic analyses

et al. 2020

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Sapajus nigritus are non-human primates which are widespread in South America. They are omnivores and live in troops of up to 40 individuals. The oral cavity is one of the main entry routes for microorganisms, including viruses. Our study proposed the identification of viral sequences from oral swabs collected in a group of capuchin monkeys (n = 5) living in a public park in a fragment of Mata Atlantica in South Brazil. Samples were submitted to nucleic acid extraction and enrichment, which was followed by the construction of libraries. After high-throughput sequencing and contig assembly, we used a pipeline to identify 11 viral families, which are Herpesviridae, Parvoviridae, Papillomaviridae, Polyomaviridae, Caulimoviridae, Iridoviridae, Astroviridae, Poxviridae, and Baculoviridae, in addition to two complete viral genomes of Anelloviridae and Genomoviridae. Some of these viruses were closely related to known viruses, while other fragments are more distantly related, with 50% of identity or less to the currently available virus sequences in databases. In addition to host-related viruses, insect and small vertebrate-related viruses were also found, as well as plant-related viruses, bringing insights about their diet. In conclusion, this viral metagenomic analysis reveals, for the first time, the profile of viruses in the oral cavity of wild, free ranging capuchin monkeys.

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Section: Discussionsupporting

confidence: 82%

Viral diversity in oral cavity from Sapajus nigritus by metagenomic analyses

et al. 2020

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“…All genomes contained five early genes (E6, E7, E1, E2, and E4), two late genes (L2 and L1), and an upstream regulatory region (URR) between L1 and E6 genes. Phylogenetic trees based on the nucleotide sequence alignment of the concatenated four open reading frames (ORFs) (E1, E2, L2, and L1) ( Fig 1 and S1 Fig ) or individual genes, e. g., E1 or L1 ORFs ( S2 Fig , S3 Fig and S4 Fig ) support a monophyletic clade grouping SscPV1/2/3 and howler monkey Alouatta guariba PV 1 (AgPV1, KP861980) [ 24 ] within the genus Dyoomikronpapillomavirus . MmPV2 and MmPV3 cluster into the genus Alphapapillomavirus , with the closest HPVs being HPV54 (within the species Alpha-13) and HPV117 (within the species Alpha-2), respectively.…”

Section: Resultsmentioning

confidence: 99%

“…Papillomaviruses have been identified in a wide range of NHP species, including Old World monkeys and apes (e.g., macaque, chimpanzee) and New World monkeys (e.g., squirrel monkey, brown howler) [ 24 , 27 – 33 ]. Using a maximal likelihood algorithm and a nucleotide sequence alignment of the concatenated E1-E2-L2-L1 ORFs for 141 PV types representing each species or unique host ( S2 Table ), we found that the majority of primate PVs phylogenetically clustered into Alphapapillomavirus , Betapapillomavirus , or Gammapapillomavirus genera, corresponding predominantly to the anatomical sites where the viruses were originally isolated (e.g., mucosal or cutaneous epithelium), which was independent of the host species ( Fig 1 , S1 Fig and S2 Table ).…”

Section: Resultsmentioning

confidence: 99%

Niche adaptation and viral transmission of human papillomaviruses from archaic hominins to modern humans

Chen¹,

DeSalle²,

Schiffman³

et al. 2018

PLoS Pathog

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Recent discoveries on the origins of modern humans from multiple archaic hominin populations and the diversity of human papillomaviruses (HPVs) suggest a complex scenario of virus-host evolution. To evaluate the origin of HPV pathogenesis, we estimated the phylogeny, timing, and dispersal of HPV16 variants using a Bayesian Markov Chain Monte Carlo framework. To increase precision, we identified and characterized non-human primate papillomaviruses from New and Old World monkeys to set molecular clock models. We demonstrate specific host niche adaptation of primate papillomaviruses with subsequent coevolution with their primate hosts for at least 40 million years. Analyses of 212 HPV16 complete genomes and 3582 partial sequences estimated ancient divergence of HPV16 variants (between A and BCD lineages) from their most recent common ancestors around half a million years ago, roughly coinciding with the timing of the split between archaic Neanderthals and modern Homo sapiens, and nearly three times longer than divergence times of modern Homo sapiens. HPV16 A lineage variants were significantly underrepresented in present African populations, whereas the A sublineages were highly prevalent in European (A1-3) and Asian (A4) populations, indicative of viral sexual transmission from Neanderthals to modern non-African humans through multiple interbreeding events in the past 80 thousand years. Remarkably, the human leukocyte antigen B*07:02 and C*07:02 alleles associated with increased risk in cervix cancer represent introgressed regions from Neanderthals in present-day Eurasians. The archaic hominin-host-switch model was also supported by other HPV variants. Niche adaptation and virus-host codivergence appear to influence the pathogenesis of papillomaviruses.

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“…2 ), a finding that may result from sampling bias. Previously described NP PVs were included in a single genus, Dyoomykronpapillomavirus , a sister clade of Alphapapillomavirus ( Silvestre et al. 2016 ; Chen et al 2018a,b ).…”

Section: Discussionmentioning

confidence: 99%

“…Human strains, accounting for 62 per cent ( n = 298) of these reports, are divided into five genera: Alpha- , Beta-, Gamma- , Mu- , and Nupapillomavirus . Only seventeen complete PV genomes infecting Old World Primates (OWP) are presently available, and more recently, four PV genomes infecting Neotropical Primates (NP) have been characterized ( Silvestre et al. 2016 ; Chen et al.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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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.

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First New World Primate Papillomavirus Identification in the Atlantic Forest, Brazil: Alouatta guariba papillomavirus 1

Abstract: We report here the complete genome sequence of the first papillomavirus detected in a New World primate, howler monkey, Alouatta guariba clamitans papillomavirus 1 (AgPV1), from the Atlantic Forest in São Paulo State, Brazil.

Cited by 13 publications

References 8 publications

Viral diversity in oral cavity from Sapajus nigritus by metagenomic analyses

Viral diversity in oral cavity from Sapajus nigritus by metagenomic analyses

Niche adaptation and viral transmission of human papillomaviruses from archaic hominins to modern humans

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

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