Papillomaviruses infecting cetaceans exhibit signs of genome adaptation following a recombination event

Abstract

Abstract Papillomaviruses (PVs) have evolved through a complex evolutionary scenario where virus–host co-evolution alone is not enough to explain the phenotypic and genotypic PV diversity observed today. Other evolutionary processes, such as host switch and recombination, also appear to play an important role in PV evolution. In this study, we have examined the genomic impact of a recombination event between distantly related PVs infecting Cetartiodactyla (even-toed ungulates and cetaceans). Our phylogenetic analyses suggest that one single recombination was responsible for the generation of extant ‘chimeric’ PV genomes infecting cetaceans. By correlating the phylogenetic relationships to the genomic content, we observed important differences between the recombinant and non-recombinant cetartiodactyle PV genomes. Notably, recombinant PVs contain a unique set of conserved motifs in the upstream regulatory region (URR). We interpret these regulatory changes as an adaptive response to drastic changes in the PV genome. In terms of codon usage preferences (CUPrefs), we did not detect any particular differences between orthologous open reading frames in recombinant and non-recombinant PVs. Instead, our results are in line with previous observations suggesting that CUPrefs in PVs are rather linked to gene expression patterns as well as to gene function. We show that the non-coding URR of PVs infecting cetaceans, the central regulatory element in these viruses, exhibits signs of adaptation following a recombination event. Our results suggest that also in PVs, the evolution of gene regulation can play an important role in speciation and adaptation to novel environments.