Assessing Host-Virus Codivergence for Close Relatives of Merkel Cell Polyomavirus Infecting African Great Apes

Abstract

It has long been hypothesized that polyomaviruses (PyV; family Polyomaviridae) codiverged with their animal hosts. In contrast, recent analyses suggested that codivergence may only marginally influence the evolution of PyV. We reassess this question by focusing on a single lineage of PyV infecting hominine hosts, the Merkel cell polyomavirus (MCPyV) lineage. By characterizing the genetic diversity of these viruses in seven African great ape taxa, we show that they exhibit very strong host specificity. Reconciliation analyses identify more codivergence than noncodivergence events. In addition, we find that a number of host and PyV divergence events are synchronous. Collectively, our results support codivergence as the dominant process at play during the evolution of the MCPyV lineage. More generally, our results add to the growing body of evidence suggesting an ancient and stable association of PyV and their animal hosts. IMPORTANCEThe processes involved in viral evolution and the interaction of viruses with their hosts are of great scientific interest and public health relevance. It has long been thought that the genetic diversity of double-stranded DNA viruses was generated over long periods of time, similar to typical host evolutionary timescales. This was also hypothesized for polyomaviruses (family Polyomaviridae), a group comprising several human pathogens, but this remains a point of controversy. Here, we investigate this question by focusing on a single lineage of polyomaviruses that infect both humans and their closest relatives, the African great apes. We show that these viruses exhibit considerable host specificity and that their evolution largely mirrors that of their hosts, suggesting that codivergence with their hosts played a major role in their diversification. Our results provide statistical evidence in favor of an association of polyomaviruses and their hosts over millions of years.

Diversity and Evolution of Novel Invertebrate DNA Viruses Revealed by Meta-Transcriptomics

“…At present, only one known invertebrate-infecting polyomavirus has been identified, Baja California bark scorpion polyomavirus 1. Other known members of the Polyomaviridae infect mammals and birds, and appear to have experienced a long period of co-evolution with their hosts [67]. We identified a novel and highly divergent polyoma-like large T antigen virus protein sequence in Trichodysplasia spinulosa spider samples and termed Spider polyomavirus ( Figure 4B).…”

Identification and Characterization of Novel Rat Polyomavirus 2 in a Colony of X-SCID Rats by P-PIT assay

“…Polyomavirus-host evolutionary studies suggest coevolution of polyomaviruses with their hosts (41). Given the broad phylogenetic radiation of polyomaviruses among rodents, it is likely that additional rat polyomaviruses are present in Rattus populations.…”

Structural Analysis of Merkel Cell Polyomavirus (MCPyV) Viral Capsid Protein 1 (VP1) in HIV-1 Infected Individuals

“…These patients often have higher titers of VP1 antibodies than normal healthy individuals [6]. Phylogenetic analysis based on the LT amino acid sequence reveals that MCPyV is most closely related to gorilla polyomavirus 1 and chimpanzee polyomaviruses 2 and 3 [18], raising the possibility that MCPyV stems from a non-human primate [18]. MCPyV may have been transmitted from apes to humans by bush meat consumption or direct contact with animals [19].…”

“…As known, VP1 is implicated in the mechanisms underlying protein self-assembly, attachment to host cell receptors, virus entry, immune response and intracellular trafficking and it plays an important role in the diagnosis of HPyVs infection and in epidemiologic studies [23][24][25][26][27]. Baez and colleagues, by an overall analysis of VP1 sequences, showed a higher variability in the N-and C-terminal regions with a characteristic deletion (∆) of six amino acids (18)(19)(20)(21)(22)(23) in the N-terminus region (aa 1-51) [21]. Kassem and colleagues, analyzing 39 MCC samples, found a 90 bp loss in the VP1 gene from one MCPyV-positive MCC sample, with an impact on the gene open reading frame [22].…”