Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2023 Apr 27;97(4):e0193222.
doi: 10.1128/jvi.01932-22. Epub 2023 Apr 6.

Evolutionarily Young African Rhinoceros Gammaretroviruses

Affiliations

Evolutionarily Young African Rhinoceros Gammaretroviruses

Kyriakos Tsangaras et al. J Virol. .

Abstract

High-throughput sequences were generated from DNA and cDNA from four Southern white rhinoceros (Ceratotherium simum simum) located in the Taronga Western Plain Zoo in Australia. Virome analysis identified reads that were similar to Mus caroli endogenous gammaretrovirus (McERV). Previous analysis of perissodactyl genomes did not recover gammaretroviruses. Our analysis, including the screening of the updated white rhinoceros (Ceratotherium simum) and black rhinoceros (Diceros bicornis) draft genomes identified high-copy orthologous gammaretroviral ERVs. Screening of Asian rhinoceros, extinct rhinoceros, domestic horse, and tapir genomes did not identify related gammaretroviral sequences in these species. The newly identified proviral sequences were designated SimumERV and DicerosERV for the white and black rhinoceros retroviruses, respectively. Two long terminal repeat (LTR) variants (LTR-A and LTR-B) were identified in the black rhinoceros, with different copy numbers associated with each (n = 101 and 373, respectively). Only the LTR-A lineage (n = 467) was found in the white rhinoceros. The African and Asian rhinoceros lineages diverged approximately 16 million years ago. Divergence age estimation of the identified proviruses suggests that the exogenous retroviral ancestor of the African rhinoceros ERVs colonized their genomes within the last 8 million years, a result consistent with the absence of these gammaretroviruses from Asian rhinoceros and other perissodactyls. The black rhinoceros germ line was colonized by two lineages of closely related retroviruses and white rhinoceros by one. Phylogenetic analysis indicates a close evolutionary relationship with ERVs of rodents including sympatric African rats, suggesting a possible African origin of the identified rhinoceros gammaretroviruses. IMPORTANCE Rhinoceros genomes were thought to be devoid of gammaretroviruses, as has been determined for other perissodactyls (horses, tapirs, and rhinoceros). While this may be true of most rhinoceros, the African white and black rhinoceros genomes have been colonized by evolutionarily young gammaretroviruses (SimumERV and DicerosERV for the white and black rhinoceros, respectively). These high-copy endogenous retroviruses (ERVs) may have expanded in multiple waves. The closest relative of SimumERV and DicerosERV is found in rodents, including African endemic species. Restriction of the ERVs to African rhinoceros suggests an African origin for the rhinoceros gammaretroviruses.

Keywords: endogenous retrovirus; evolution; gammaretrovirus; perissodactyl; rhinoceros.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIG 1
FIG 1
Multiple alignment of SimumERV and DicerosERV consensus sequences from white rhinoceros next-generation sequencing data (SimumERV_cons), white rhinoceros (SimumERV), and black rhinoceros (DicerosERV) genomes. Sequences are annotated indicating the location of LTRs in light blue, primer binding sites (PBSs) are in yellow, proviral genes gag, pro, pol, and env are illustrated in green, and identified pathogenicity and conserved domain motifs are illustrated in pink. The four sequences have an average pairwise nucleotide identity of 86.3%. Sequence differences among the sequences are indicated by black vertical lines.
FIG 2
FIG 2
Phylogenetic relationship of SimumERV and DicerosERV LTR sequences. The unrooted maximum likelihood tree illustrates the 463 SimumERV and 470 DicerosERV proviral and solitary LTR sequences identified in white and black rhinoceros genomes excluding sequence outliers. Black clades represent SimumERV LTRs, orange clades represent DicerosERV LTR-A, and green clades represent DicerosERV LTR-B. Sequences that were identified in BLASTn searches as related to the rhinoceros ERVs but that aligned very poorly and may represent false hits were excluded from the analysis. However, sequences that did align well along the proviral sequence but were more divergent from other proviral sequences for shorter internal regions were not excluded as outliers and are visible as long branches.
FIG 3
FIG 3
Boxplots illustrating age estimations of SimumERV and DicerosERV loci using multiple approaches. For more accurate age estimations, ERV sequence alignments were separated into subgroups based on sequence similarity. Age estimations were performed comparing the gag, pol, and env gene regions of each provirus as well as LTRs (solitary and proviral; “con”) to the consensus sequences of its respective subgroup. Furthermore, provirus ages were estimated via the number of nucleotide differences between individual proviral 5′ to 3′ LTRs. Individual ERV locus (proviruses, solitary LTRs) age estimations are illustrated with black dots next to each subgroup’s boxplot. Black lines indicate the median age, squares indicate the mean, and whiskers indicate the 1.5-fold interquartile range.
FIG 4
FIG 4
Phylogenetic analysis of SimumERV and DicerosERV consensus nucleotide whole-genome sequences excluding LTRs within the family Retroviridae. A phylogenetic tree was constructed using RAxML and the GTR gamma substitution model with 20 maximum likelihood searches and 500 rapid bootstrap replicates. Bootstrap support is given at nodes. Reticuloendotheliosis virus was used as an outgroup. The scale bar represents nucleotide substitutions per site.

References

    1. Johnson WE. 2015. Endogenous retroviruses in the genomics era. Annu Rev Virol 2:135–159. doi: 10.1146/annurev-virology-100114-054945. - DOI - PubMed
    1. Johnson WE. 2019. Origins and evolutionary consequences of ancient endogenous retroviruses. Nat Rev Microbiol 17:355–370. doi: 10.1038/s41579-019-0189-2. - DOI - PubMed
    1. Tsangaras K, Mayer J, Alquezar-Planas DE, Greenwood AD. 2015. An evolutionarily young polar bear (Ursus maritimus) endogenous retrovirus identified from next generation sequence data. Viruses 7:6089–6107. doi: 10.3390/v7112927. - DOI - PMC - PubMed
    1. Gifford R, Tristem M. 2003. The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26:291–315. doi: 10.1023/a:1024455415443. - DOI - PubMed
    1. Mayer J, Tsangaras K, Heeger F, Ávila-Arcos M, Stenglein MD, Chen W, Sun W, Mazzoni CJ, Osterrieder N, Greenwood AD. 2013. A novel endogenous betaretrovirus group characterized from polar bears (Ursus maritimus) and giant pandas (Ailuropoda melanoleuca). Virology 443:1–10. doi: 10.1016/j.virol.2013.05.008. - DOI - PMC - PubMed

LinkOut - more resources