Extensive retroviral diversity in shark

Han, Guan-Zhu

doi:10.1186/s12977-015-0158-4

Cited by 18 publications

(14 citation statements)

References 16 publications

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“…The most prominent examples of EVEs are endogenous retroviruses that can be found in most vertebrate species (47). Even the coelacanth and elephant shark genomes contain a high diversity of endogenous retroviruses as remnants of ancient infections (48,49). In addition to retroviral elements, many bird and mammal species also contain EVEs related to hepadna-or filoviruses (46).…”

Section: Discussionmentioning

confidence: 99%

Early Vertebrate Evolution of the Host Restriction Factor Tetherin

Heusinger

Kluge

Kirchhoff

et al. 2015

J Virol

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Tetherin is an interferon-inducible restriction factor targeting a broad range of enveloped viruses. Its antiviral activity depends on an unusual topology comprising an N-terminal transmembrane domain (TMD) followed by an extracellular coiled-coil region and a C-terminal glycosylphosphatidylinositol (GPI) anchor. One of the two membrane anchors is inserted into assembling virions, while the other remains in the plasma membrane of the infected cell. Thus, tetherin entraps budding viruses by physically bridging viral and cellular membranes. Although tetherin restricts the release of a large variety of diverse human and animal viruses, only mammalian orthologs have been described to date. Here, we examined the evolutionary origin of this protein and demonstrate that tetherin orthologs are also found in fish, reptiles, and birds. Notably, alligator tetherin efficiently blocks the release of retroviral particles. Thus, tetherin emerged early during vertebrate evolution and acquired its antiviral activity before the mammal/reptile divergence. Although there is only limited sequence homology, all orthologs share the typical topology. Two unrelated proteins of the slime mold Dictyostelium discoideum also adopt a tetherin-like configuration with an N-terminal TMD and a C-terminal GPI anchor. However, these proteins showed no evidence for convergent evolution and failed to inhibit virion release. In summary, our findings demonstrate that tetherin emerged at least 450 million years ago and is more widespread than previously anticipated. The early evolution of antiviral activity together with the high topology conservation but low sequence homology suggests that restriction of virus release is the primary function of tetherin. IMPORTANCEThe continuous arms race with viruses has driven the evolution of a variety of cell-intrinsic immunity factors that inhibit different steps of the viral replication cycle. One of these restriction factors, tetherin, inhibits the release of newly formed progeny virions from infected cells. Although tetherin targets a broad range of enveloped viruses, including retro-, filo-, herpes-, and arenaviruses, the evolutionary origin of this restriction factor and its antiviral activity remained obscure. Here, we examined diverse vertebrate genomes for genes encoding cellular proteins that share with tetherin the highly unusual combination of an N-terminal transmembrane domain and a C-terminal glycosylphosphatidylinositol anchor. We show that tetherin orthologs are found in fish, reptiles, and birds and demonstrate that alligator tetherin efficiently inhibits the release of retroviral particles. Our findings identify tetherin as an evolutionarily ancient restriction factor and provide new important insights into the continuous arms race between viruses and their hosts.

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Section: Discussionmentioning

confidence: 99%

Early Vertebrate Evolution of the Host Restriction Factor Tetherin

Heusinger

Kluge

Kirchhoff

et al. 2015

J Virol

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“…For example, the identification of endogenous foamy virus in fishes reveals an ancient marine origin of this retroviral group, and possibly the whole retroviruses [ 10 , 18 , 19 ]. Several attempts to mine ERVs in some non-avian/mammalian vertebrate genomes have been made [ 16 , 20 – 22 ], but these genome-scale surveys exploited only very limited number of species (one to around ten).…”

Section: Introductionmentioning

confidence: 99%

Endogenous retroviruses of non-avian/mammalian vertebrates illuminate diversity and deep history of retroviruses

Zhao

Gong

et al. 2018

PLoS Pathog

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The deep history and early diversification of retroviruses remains elusive, largely because few retroviruses have been characterized in vertebrates other than mammals and birds. Endogenous retroviruses (ERVs) documented past retroviral infections and thus provide ‘molecular fossils’ for studying the deep history of retroviruses. Here we perform a comprehensive phylogenomic analysis of ERVs within the genomes of 92 non-avian/mammalian vertebrates, including 72 fishes, 4 amphibians, and 16 reptiles. We find that ERVs are present in all the genomes of jawed vertebrates, revealing the ubiquitous presence of ERVs in jawed vertebrates. We identify a total of >8,000 ERVs and reconstruct ~450 complete or partial ERV genomes, which dramatically expands the phylogenetic diversity of retroviruses and suggests that the diversity of exogenous retroviruses might be much underestimated in non-avian/mammalian vertebrates. Phylogenetic analyses show that retroviruses cluster into five major groups with different host distributions, providing important insights into the classification and diversification of retroviruses. Moreover, we find retroviruses mainly underwent frequent host switches in non-avian/mammalian vertebrates, with exception of spumavirus-related viruses that codiverged with their ray-finned fish hosts. Interestingly, ray-finned fishes and turtles appear to serve as unappreciated hubs for the transmission of retroviruses. Finally, we find retroviruses underwent many independent water-land transmissions, indicating the water-land interface is not a strict barrier for retrovirus transmission. Our analyses provide unprecedented insights into and valuable resources for studying the diversification, key evolutionary transitions, and macroevolution of retroviruses.

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“…It is well known that the nucleotide difference between the 5′ and 3′ LTR sequences of a single GGERV10 element resulted from point mutations after insertion [21]. Therefore, the nucleotide difference between the 5′ and 3′ LTR sequences could be used to estimate the ERV insertion time [22]. To estimate the age of the GGERV10 subfamilies, we performed the NETWORK analysis [23], based on the evolutionary divergence between all LTR sequences of each subfamily (Additional file 6: Table S4).…”

Section: Resultsmentioning

confidence: 99%

Chicken (Gallus gallus) endogenous retrovirus generates genomic variations in the chicken genome

et al. 2017

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BackgroundTransposable elements (TEs) comprise ~10% of the chicken (Gallus gallus) genome. The content of TEs is much lower than that of mammalian genomes, where TEs comprise around half of the genome. Endogenous retroviruses are responsible for ~1.3% of the chicken genome. Among them is Gallus gallus endogenous retrovirus 10 (GGERV10), one of the youngest endogenous retrovirus families, which emerged in the chicken genome around 3 million years ago.ResultsWe identified a total of 593 GGERV10 elements in the chicken reference genome using UCSC genome database and RepeatMasker. While most of the elements were truncated, 49 GGERV10 elements were full-length retaining 5′ and 3′ LTRs. We examined in detail their structural features, chromosomal distribution, genomic environment, and phylogenetic relationships. We compared LTR sequence among five different GGERV10 subfamilies and found sequence variations among the LTRs. Using a traditional PCR assay, we examined a polymorphism rate of the 49 full-length GGERV10 elements in three different chicken populations of the Korean domestic chicken, Leghorn, and Araucana. The result found a breed-specific GGERV10B insertion locus in the Korean domestic chicken, which could be used as a Korean domestic chicken-specific marker.ConclusionsGGERV10 family is the youngest ERV family and thus might have contributed to recent genomic variations in different chicken populations. The result of this study showed that one of GGERV10 elements integrated into the chicken genome after the divergence of Korean domestic chicken from other closely related chicken populations, suggesting that GGERV10 could be served as a molecular marker for chicken breed identification.Electronic supplementary materialThe online version of this article (doi:10.1186/s13100-016-0085-5) contains supplementary material, which is available to authorized users.

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Extensive retroviral diversity in shark

Cited by 18 publications

References 16 publications

Early Vertebrate Evolution of the Host Restriction Factor Tetherin

Early Vertebrate Evolution of the Host Restriction Factor Tetherin

Endogenous retroviruses of non-avian/mammalian vertebrates illuminate diversity and deep history of retroviruses

Chicken (Gallus gallus) endogenous retrovirus generates genomic variations in the chicken genome

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