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. 2018 Aug 29;92(18):e00980-18.
doi: 10.1128/JVI.00980-18. Print 2018 Sep 15.

DNA Polymerase Sequences of New World Monkey Cytomegaloviruses: Another Molecular Marker with Which To Infer Platyrrhini Systematics

Samantha James  1   2 , Damien Donato  1 , Jean-François Pouliquen  1 , Manuel Ruiz-García  3 , Anne Lavergne  1   2 , Vincent Lacoste  4   2   5
Affiliations

DNA Polymerase Sequences of New World Monkey Cytomegaloviruses: Another Molecular Marker with Which To Infer Platyrrhini Systematics

Samantha James et al. J Virol. .

Abstract

Over the past few decades, a large number of studies have identified herpesvirus sequences from many mammalian species around the world. Among the different nonhuman primate species tested so far for cytomegaloviruses (CMVs), only a few were from the New World. Seeking to identify CMV homologues in New World monkeys (NWMs), we carried out molecular screening of 244 blood DNA samples from 20 NWM species from Central and South America. Our aim was to reach a better understanding of their evolutionary processes within the Platyrrhini parvorder. Using PCR amplification with degenerate consensus primers targeting highly conserved amino acid motifs encoded by the herpesvirus DNA polymerase gene, we characterized novel viral sequences from 12 species belonging to seven genera representative of the three NWM families. BLAST searches, pairwise nucleotide and amino acid sequence comparisons, and phylogenetic analyses confirmed that they all belonged to the Cytomegalovirus genus. Previously determined host taxa allowed us to demonstrate a good correlation between the distinct monophyletic clades of viruses and those of the infected primates at the genus level. In addition, the evolutionary branching points that separate NWM CMVs were congruent with the divergence dates of their hosts at the genus level. These results significantly expand our knowledge of the host range of this viral genus and strongly support the occurrence of cospeciation between these viruses and their hosts. In this respect, we propose that NWM CMV DNA polymerase gene sequences may serve as reliable molecular markers with which to infer Platyrrhini phylogenetics.IMPORTANCE Investigating evolutionary processes between viruses and nonhuman primates has led to the discovery of a large number of herpesviruses. No study published so far on primate cytomegaloviruses has extensively studied New World monkeys (NWMs) at the subspecies, species, genus, and family levels. The present study sought to identify cytomegalovirus homologues in NWMs and to decipher their evolutionary relationships. This led us to characterize novel viruses from 12 of the 20 primate species tested, which are representative of the three NWM families. The identification of distinct viruses in these primates not only significantly expands our knowledge of the host range of this viral genus but also sheds light on its evolutionary history. Phylogenetic analyses and molecular dating of the sequences obtained support a virus-host coevolution.

Keywords: CMV; Cytomegalovirus; New World monkeys; evolution; phylogeny.

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Figures

FIG 1
FIG 1
Diagram representation of Platyrrhini taxa in descending order down to the genus level. Black and gray boxes represent NWM genera tested for CMVs. Black boxes correspond to NWM genera from which CMV sequences have been characterized, while gray boxes represent NWM genera from which no CMV sequence was obtained in the present study. (Adapted from reference with permission of the publisher.)
FIG 2
FIG 2
Relative positions and orientations of the PCR primers used in this study. The different combinations of primers used in nested or seminested PCRs are represented above the herpesviral DNA polymerase gene sequence, in different gray boxes. Primers XxxR1 and XxxR2, represented by dotted arrows, correspond to the different antisense specific primers used in a degenerate (CMV2F1 or CMV2F2)-nondegenerate nPCR assay (Table 2). Bars below the sequence represent the different nested PCR products expected. The pairs of primers on the left side of the bars indicate those used for the first-round PCR, while those on the right side correspond to those used in the nested PCRs. The sequences of the oligonucleotide primers are given in Table 2.
FIG 3
FIG 3
Phylogenetic analysis of primate cytomegalovirus sequences. The phylogenetic tree was derived from the partial amino acid sequences of the DNA polymerase genes (149 aa) of 50 representatives of primate cytomegaloviruses, using the Bayesian method with the JTT+G model of amino acid evolution. Sequences generated in this study are shown in bold. Posterior probabilities of the Bayesian analysis (>0.9) are shown next to the nodes. The scale bar indicates the number of amino acid substitutions per site. The major clades representing Old World and New World primate families, superfamilies (for OWM), and parvorders are labeled on the right side of the figure. The virus names are associated with their accession numbers. Viruses of the Cercopithecidae comprise those of the chacma (BaCMV NC_027016 [21, 59]) and olive (BaCMV AF387664 [22]) baboons, the moustached guenon (CceCMV1 AY728178), the agile mangabey (CagCMV1 AY608713), the drill (MndCMV AF282941 and MndCMV AF387665 [strain OCOM6-2] [22, 28]), the mandrill (MndCMV AY129399), the African green monkey (CeHV5 AY117754, CeHV5 FJ483969 [strain Colburn], CeHV5 FJ483969 [strain 2715], CaeCMV AF292066, VervetCMV AY049066 [strain CSG], and CeHV3 AY049065 [22, 60]), the cynomolgus macaque (MfasCMV1 JN227533 [strain Ottawa], MfasCMV1 AY728171, and MfasCMV KP796148 [strain Mauritius] [61, 62]), the rhesus macaque (McHV3 AF033184 and McHV3 DQ120516 [isolate CMV 180.92] [63, 64]), and the mantled guereza (CgueCMV1.1 AY129397 and CgueCMV1.2 EU118147 [30]). Viruses of the Hominidae comprise those of the Bornean orangutan (PpygCMV1.1 AY129396), the human (HHV5 M14709 [strain AD169], HHV5 NC_006273 [strain Merlin], HHV5 AY315197 [strain Towne], and HHV5 AC146905 [isolate Toledo] [65–68]), the Western gorilla (GgorCMV2.1 FJ538490 [27]), and the common chimpanzee (PnHV2 AF480884 [strain Heberling], PtroCMV1.1 FJ538485, and PtroCMV AF292063 [27, 66]). Regarding viruses of New World monkeys, in addition to those described in the present study, viruses of the Cebidae comprise those of the capuchin monkey (CebHV1 JQ264772 and CebusHV AF292067 [from Cebus spp.]), the common squirrel monkey (SaHV4 FJ483967 and SscHV AF292065), and the three-striped night monkey (AoHV1 FJ483970).
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