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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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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.
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Fig1: 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.

Mentions: In the phylogenetic reconstruction using the RT fragment (Figure 1), the most abundant elements were represented by Gammaretrovirus-like (class I) sequences. Sequences belonging to class II ERVs and a divergent sequence (LwiJO7007), distantly related to the RV-Tuatara endogenous retrovirus [17], were also observed. Additionally, in a search for ERVs using Censor [18], a sequence from L. wiedii (LwiCT12006) showed 68% identity with ERV3-16A3_I, an ERV3-type (class III) endogenous retrovirus. This L. wiedii sequence was excluded from further analysis because it did not contain an identifiable RT domain. We did not find any sequences similar to exogenous retroviruses such as FIV and FFV among the 236 analyzed clones. Likewise, in Blastn searches against the Panthera tigris and Felis catus WGS database (as of October 2013) using gag, pol and env genes from FIV [GenBank: M25381.1] and from FFV [GenBank: Y08851.1] as query sequences, no ERV sequence presenting and e-value < 0.001 was retrieved in these genomes.Figure 1


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

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

Fig1: 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.
Mentions: In the phylogenetic reconstruction using the RT fragment (Figure 1), the most abundant elements were represented by Gammaretrovirus-like (class I) sequences. Sequences belonging to class II ERVs and a divergent sequence (LwiJO7007), distantly related to the RV-Tuatara endogenous retrovirus [17], were also observed. Additionally, in a search for ERVs using Censor [18], a sequence from L. wiedii (LwiCT12006) showed 68% identity with ERV3-16A3_I, an ERV3-type (class III) endogenous retrovirus. This L. wiedii sequence was excluded from further analysis because it did not contain an identifiable RT domain. We did not find any sequences similar to exogenous retroviruses such as FIV and FFV among the 236 analyzed clones. Likewise, in Blastn searches against the Panthera tigris and Felis catus WGS database (as of October 2013) using gag, pol and env genes from FIV [GenBank: M25381.1] and from FFV [GenBank: Y08851.1] as query sequences, no ERV sequence presenting and e-value < 0.001 was retrieved in these genomes.Figure 1

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