Dataset Information

Genome-Wide Characterization of Zebrafish Endogenous Retroviruses Reveals Unexpected Diversity in Genetic Organizations and Functional Potentials.

ABSTRACT: Endogenous retroviruses (ERVs) occupy a substantial fraction of mammalian genomes. However, whether ERVs extensively exist in ancient vertebrates remains unexplored. Here, we performed a genome-wide characterization of ERVs in a zebrafish (Danio rerio) model. Approximately 3,315 ERV-like elements (DrERVs) were identified as Gypsy, Copia, Bel, and class I-III groups. DrERVs accounted for approximately 2.3% of zebrafish genome and were distributed in all 25 chromosomes, with a remarkable bias on chromosome 4. Gypsy and class I are the two most abundant groups with earlier insertion times. The vast majority of the DrERVs have varied structural defects. A total of 509 gag and 71 env genes with coding potentials were detected. The env-coding elements were well-characterized and classified into four subgroups. A ERV-E4.8.43-DanRer element shows high similarity with HERV9NC-int in humans and analogous sequences were detected in species spanning from fish to mammals. RNA-seq data showed that hundreds of DrERVs were expressed in embryos and tissues under physiological conditions, and most of them exhibited stage and tissue specificity. Additionally, 421 DrERVs showed strong responsiveness to virus infection. A unique group of DrERVs with immune-relevant genes, such as fga, ddx41, ftr35, igl1c3, and tbk1, instead of intrinsic viral genes were identified. These DrERVs are regulated by transcriptional factors binding at the long terminal repeats. This study provided a survey of the composition, phylogeny, and potential functions of ERVs in a fish model, which benefits the understanding of the evolutionary history of ERVs from fish to mammals. IMPORTANCE Endogenous retroviruses (ERVs) are relics of past infection that constitute up to 8% of the human genome. Understanding the genetic evolution of the ERV family and the interplay of ERVs and encoded RNAs and proteins with host function has become a new frontier in biology. Fish, as the most primitive vertebrate host for retroviruses, is an indispensable integral part for such investigations. In the present study, we report the genome-wide characterization of ERVs in zebrafish, an attractive model organism of ancient vertebrates from multiple perspectives, including composition, genomic organization, chromosome distribution, classification, phylogeny, insertion time, characterization of gag and env genes, and expression profiles in embryos and tissues. The result helps uncover the evolutionarily conserved and fish-specific ERVs, as well as the immune-relevant ERVs in response to virus infection. This study demonstrates the previously unrecognized abundance, diversification, and extensive activity of ERVs at the early stage of ERV evolution.

SUBMITTER: Bai J

PROVIDER: S-EPMC8672886 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

Project description:Endogenous retroviruses (ERVs) are the remnants of past retroviral infections. Fossil records of class II retroviruses have been discovered in a range of vertebrates, with the exception of amphibians, which are known only to possess class I and class III-like ERVs. Through genomic mining of all available amphibian genomes, we identified, for the first time, class II ERVs in amphibians. The class II ERVs were found only in Gymnophiona (caecilians) and not in the genomes of the other amphibian orders, Anura (frogs and toads) and Caudata (salamanders and newts), which are phylogenetically closely related. Therefore, the ERV endogenization occurred after the split of Gymnophiona, Anura, and Caudata (323 million years ago). Investigation of phylogenetic relationship and genomic structure revealed that the ERVs may originate from alpha- or betaretroviruses. We offer evidence that class II ERVs infiltrated amphibian genomes recently and may still have infectious members. Remarkably, certain amphibian class II ERVs can be expressed in diverse tissues. This discovery closes the major gap in the retroviral fossil record of class II ERVs and provides important insights into the evolution of class II ERVs in vertebrates.IMPORTANCE Class II retroviruses, largely distributed among mammals and birds, are of particular importance for medicine and economics. Class II ERVs have been discovered in a range of vertebrates, with the exception of amphibians, which are known only to possess class I and class III-like ERVs. Here, for the first time, we discovered class II ERVs in amphibians. We also revealed that the ERVs may originate from alpha- or betaretroviruses. We revealed that class II ERVs were integrated into amphibian genomes recently and certain amphibian class II ERVs can be expressed in diverse tissues. Our discovery closes the major gap in the retroviral fossil record of class II ERVs, and also indicates that amphibians may be still infected by class II retroviruses.

Project description:BackgroundEndogenous retroviruses (ERV) are remnants of former exogenous retroviruses that had previously invaded the germ line of the host that can be vertically transmitted across generations. While the majority of ERVs lack infectious capacity due to the accumulation of deleterious mutations, some ERVs remain active and produce potentially infectious viral particles. ERV sequences have been reported in all mammals; however, the distribution and diversity of ERVs in several primate taxa remains unclear. The aim of this study was to identify and classify the ERV sequences in the genomes of the golden snub-nosed monkey (Rhinopithecus roxellana) and the black and white snub-nosed monkey (Rhinopithecus bieti), two endangered primate species that exploit high altitude (2,500-4,500 m) temperate forests in southern and central China.MethodsWe used a TBLASTN program to search the ERV sequences of golden snub-nosed monkey genome and the black and white snub-nosed monkey genome. We retrieved all complete accession sequences from the homology search and then used the program, RetroTector, to check and identify the ERV sequences.ResultsWe identified 284 and 263 endogenous retrovirus sequences in R. roxellana and R. bieti respectively. The proportion of full-length sequences of all ERV was 30% in R. roxellana and 21% in R. bieti and they were described as class I and class II or gamma-retrovirus and beta-retrovirus genera. The truncation pattern distribution in the two species was virtually identical. By analyzing and comparing ERV orthologues among 6 primate species, we identified the co-evolution of ERVs with their host. We also examined ERV-like sequences and found 48 such genes in R. roxellana and 63 in R. bieti. Some of those genes are associated with diseases, suggesting that ERVs might have involved the abnormal expression of certain genes that have contributed to deleterious consequences for the host.ConclusionsOur results indicate that ERV sequences are widely distributed in snub-nosed monkeys, and their phylogenetic history can mirror that of their hosts over long evolutionary time scales. In addition, ERV sequences appear to have an important influence on the evolution of host pathology.

Dataset Information

Genome-Wide Characterization of Zebrafish Endogenous Retroviruses Reveals Unexpected Diversity in Genetic Organizations and Functional Potentials.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets