Identification and characterization of diverse groups of endogenous retroviruses in felids

Abstract

Background: Endogenous retroviruses (ERVs) are genetic elements with a retroviral origin that are integrated into vertebrate genomes. In felids (Mammalia, Carnivora, Felidae), ERVs have been described mostly in the domestic cat, and only rarely in wild species. To gain insight into the origins and evolutionary dynamics of endogenous retroviruses in felids, we have identified and characterized partial pro/pol ERV sequences from eight Neotropical wild cat species, belonging to three distinct lineages of Felidae. We also compared them with publicly available genomic sequences of Felis catus and Panthera tigris, as well as with representatives of other vertebrate groups, and performed phylogenetic and molecular dating analyses to investigate the pattern and timing of diversification of these retroviral elements.

Results: We identified a high diversity of ERVs in the sampled felids, with a predominance of Gammaretrovirus-related sequences, including class I ERVs. Our data indicate that the identified ERVs arose from at least eleven horizontal interordinal transmissions from other mammals. Furthermore, we estimated that the majority of the Gamma-like integrations took place during the diversification of modern felids. Finally, our phylogenetic analyses indicate the presence of a genetically divergent group of sequences whose position in our phylogenetic tree was difficult to establish confidently relative to known retroviruses, and another lineage identified as ERVs belonging to class II.

Conclusions: Retroviruses have circulated in felids along with their evolution. The majority of the deep clades of ERVs exist since the primary divergence of felids' base and cluster with retroviruses of divergent mammalian lineages, suggesting horizontal interordinal transmission. Our findings highlight the importance of additional studies on the role of ERVs in the genome landscaping of other carnivore species.

Figure 1

Phylogenetic tree showing the diversity of felid endogenous retroviruses. Maximum likelihood tree was based on deduced amino acid sequences of an RT fragment (Dataset1; 147 codons). Bootstrap values > 70% are indicated next to respective nodes (omitted for clarity on terminal branches). Host species’ designations are according to the inset graphical legend. G1 to G3 in red refer to distinct Gammaretrovirus groups identified based on the phylogenetic results and Gamma1-9 were previously described by Song et al. [14]. Exogenous retroviruses and their respective genera are in green. Retroviral sequences retrieved from GenBank are listed in Additional file 1: Table S1. The scale bar at the bottom represents the evolutionary distance in amino acid substitutions per site.

Figure 2

Phylogenetic relationships among DNA sequences most closely related to LwiJO7007. A maximum likelihood tree was constructed with a 613 bp-long alignment (Dataset 2). Bootstrap values > 70% are indicated next to their respective nodes. Mammalian orders containing sampled sequences are indicated above the branches defining each lineage. Felid illustrations are shown to designate their clades. Tiger is represented in blue, domestic cat in red and L. wiedii in green. The scale bar at the bottom represents distance in nucleotide substitutions per site. All sequences are listed in Table 1 and Additional file 1: Table S1.

Figure 3

Phylogenetic tree showing the diversity of felid gammaretroviruses. A maximum likelihood tree was based on deduced amino acids of Pro-Pol fragments (Dataset 3; 198 codons). Bootstrap values > 70% are shown next to respective branches. The WGS sequences from Panthera tigris altaica [GenBank: ATCQ01000000], Felis catus [GenBank: AANG00000000] (Abyssinian breed) and [GenBank: ACBE00000000] (mixed breed) are indicated. Puma concolor (sequences starting with Pco), P. yagouaroundi (Py), L. geoffroyi (Lg), L. colocolo (Lco), L. guttulus (Lgu), L. pardalis (LP), L. wiedii (Lwi) and P. onca (OC) are also depicted. Roman numbers I to XI represent distinct Gamma-like retroviral lineages characterized in this study (marked in red). Asterisks indicate sequences mentioned in Table 2. The scale bar at the bottom of the Figure represents distance in amino acid substitutions per site. Sequences retrieved from GenBank are listed in Additional file 1: Table S1. ERVs termed Gamma1-9 by Song et al. [14] are indicated with the # symbol.

Figure 4

Phylogenetic tree showing the relationships of class II ERV sequences. A maximum likelihood tree was based on deduced amino acids of Pro-Pol fragments (Dataset 4; 236 codons). Bootstrap values >70% are indicated. Felid illustrations are shown to designate their clades. The three ERV clades mentioned in the text are highlighted by showing sequences from four of the major felid lineages: blue (from tiger belonging to the Panthera lineage), red (cat, domestic cat lineage), green (PYEM13001, from P. yagouaroundi and Puma concolor, both from the Puma lineage) and pink (L. geoffroyi, ocelot lineage). The scale bar at the bottom of the Figure represents distance in amino acid substitutions per site. Sequences retrieved from GenBank are listed in Additional file 1: Table S1.