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

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.

SUBMITTER: Borveto F

PROVIDER: S-EPMC7326301 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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

Borvető Fanni F Bravo Ignacio G IG Willemsen Anouk A

Virus evolution 20200101 1

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 phylogen ...[more]

PMID: 32665861

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Project description:BackgroundOsmoregulation was a primary challenge for cetaceans during the evolutionary transition from a terrestrial to a mainly hyperosmotic environment. Several physiological mechanisms have been suggested to maintain the water and salt balance in cetaceans, but their genetic and evolutionary bases remain poorly explored. The current study investigated the genes involved in osmoregulation in cetaceans and compared them with their counterparts in terrestrial mammals to test whether adaptive evolution occurred during secondary aquatic adaptation.ResultsThe present study analyzed the molecular evolution of 11 osmoregulation-related genes in 11 cetacean species, which represented all of the major cetacean clades. The results demonstrated positive selection acting on angiotensin converting enzyme (ACE), angiotensinogen (AGT), SLC14A2, and aquaporin 2 (AQP2). This evidence for the positive selection of AQP2 and SLC14A2 suggests that the adaptive evolution of these genes has helped to enhance the capacity for water and urea transport, thereby leading to the concentration of urine, which is an efficient mechanism for maintaining the water balance. By contrast, a series of positively selected amino acid residues identified in the ACE and AGT (two key members of the renin-angiotensin-aldosterone system, RAAS) proteins of cetaceans suggests that RAAS might have been adapted to maintain the water and salt balance in response to a hyperosmotic environment. Radical amino acid changes in positively selected sites were distributed among most internal and terminal branches of the cetacean phylogeny, which suggests the pervasively adaptive evolution of osmoregulation since the origin of cetaceans and their subsequent diversification.ConclusionsThis is the first comprehensive analysis of the molecular evolution of osmoregulation-related genes in cetaceans in response to selection pressure from a generally hyperosmotic environment. Four genes, i.e., AQP2, SLC14A2, ACE, and AGT were subject to positive selection in cetaceans, which suggests that cetaceans may have adapted to maintain their water and salt balance. This also suggests that cetaceans may have evolved an effective and complex mechanism for osmoregulation.

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

Publications

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

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