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Identification and characterization of diverse groups of endogenous retroviruses in felids.

Mata H, Gongora J, Eizirik E, Alves BM, Soares MA, Ravazzolo AP - Retrovirology (2015)

Bottom Line: 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.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.Our findings highlight the importance of additional studies on the role of ERVs in the genome landscaping of other carnivore species.

View Article: PubMed Central - PubMed

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.

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Related in: MedlinePlus

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.
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Fig2: 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.

Mentions: The RT phylogeny depicted in Figure 1 shows the sequence of clone LwiJO7007 clustering closely with a sequence from the domestic cat, jointly forming a highly divergent group. A Blastn search using LwiJO7007 as a query sequence against the Retroviridae database did not retrieve any sequence similar to a known retrovirus. When using Blastx, the seven top hits corresponded to Epsilonretrovirus sequences, showing identities ranging between 31 and 34% (e-values < 10-13, queries covering > 92%). The Blastx search showed that 441 out of 641 nts belonged to the RT-like superfamily. A RepeatMasker analysis indicated that this retroelement is 67% identical to the shared segment of CarERV4-int, which was categorized as belonging to the ERV1 family (ERV Class I). In spite of its distant relationship to known/annotated ERVs, Blastn searches using LwiJO7007 against WGS databases revealed the existence of closely-related sequences (71-95% identity) in the genomes of domestic cat, tiger and several other mammals, encompassing four different placental orders (Figure 2 and Table 1). Sequences from specific PCR (LwiJO7007 group) showed that all species of Brazilian wild cats tested positive for this retroviral element (Additional file 2: Figure S1).Figure 2


Identification and characterization of diverse groups of endogenous retroviruses in felids.

Mata H, Gongora J, Eizirik E, Alves BM, Soares MA, Ravazzolo AP - Retrovirology (2015)

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.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4373062&req=5

Fig2: 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.
Mentions: The RT phylogeny depicted in Figure 1 shows the sequence of clone LwiJO7007 clustering closely with a sequence from the domestic cat, jointly forming a highly divergent group. A Blastn search using LwiJO7007 as a query sequence against the Retroviridae database did not retrieve any sequence similar to a known retrovirus. When using Blastx, the seven top hits corresponded to Epsilonretrovirus sequences, showing identities ranging between 31 and 34% (e-values < 10-13, queries covering > 92%). The Blastx search showed that 441 out of 641 nts belonged to the RT-like superfamily. A RepeatMasker analysis indicated that this retroelement is 67% identical to the shared segment of CarERV4-int, which was categorized as belonging to the ERV1 family (ERV Class I). In spite of its distant relationship to known/annotated ERVs, Blastn searches using LwiJO7007 against WGS databases revealed the existence of closely-related sequences (71-95% identity) in the genomes of domestic cat, tiger and several other mammals, encompassing four different placental orders (Figure 2 and Table 1). Sequences from specific PCR (LwiJO7007 group) showed that all species of Brazilian wild cats tested positive for this retroviral element (Additional file 2: Figure S1).Figure 2

Bottom Line: 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.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.Our findings highlight the importance of additional studies on the role of ERVs in the genome landscaping of other carnivore species.

View Article: PubMed Central - PubMed

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.

Show MeSH
Related in: MedlinePlus