Endogenous retroviruses are a common ancestral feature of mammalian genomes with most having been inactivated over time through mutation and deletion1. A group of more intact endogenous retroviruses are considered to have entered the genomes of some species more recently, through infection by exogenous viruses2, but this event has never been directly proved. We have previously reported koala retrovirus (KoRV) to be a functional virus that is associated with neoplasia3. Here we show that KoRV also shows features of a recently inserted endogenous retrovirus that is vertically transmitted. The finding that some isolated koala populations have not yet incorporated KoRV into their genomes, combined with its high level of activity and variability in individual koalas, suggests that KoRV is a virus in transition between an exogenous and endogenous element. This ongoing dynamic interaction with a wild species provides an exciting opportunity to study the process and consequences of retroviral endogenization in action, and is an attractive model for studying the evolutionary event in which a retrovirus invades a mammalian genome.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Taruscio, D. & Mantovani, A. Factors regulating endogenous retroviral sequences in human and mouse. Cytogenet. Genome Res. 105, 2–4 (2004)
Boeke, J. D. & Stoye, J. P. in Retroviruses (eds Coffin, J. M., Hughes, S. H. & Varmus, H. E.) 343–346 (Cold Spring Harbor Laboratory Press, New York, 1997)
Tarlinton, R., Meers, J., Hanger, J. & Young, P. Real-time reverse transcriptase PCR for the endogenous koala retrovirus reveals an association between plasma viral load and neoplastic disease in koalas. J. Gen. Virol. 86, 783–787 (2005)
Hanger, J. J., Bromham, L. D., McKee, J. J., O'Brien, T. M. & Robinson, W. F. The nucleotide sequence of koala (Phascolarctos cinereus) retrovirus: a novel type C endogenous virus related to gibbon ape leukemia virus. J. Virol. 74, 4264–4272 (2000)
Herniou, E. et al. Retroviral diversity and distribution in vertebrates. J. Virol. 72, 5955–5966 (1998)
Resnick, R. M., Boyce-Jacino, M. T., Fu, Q. & Faras, A. J. Phylogenetic distribution of the novel avian endogenous provirus family EAV-0. J. Virol. 64, 4640–4653 (1990)
Carlson, J. et al. Chromosomal distribution of endogenous Jaagsietkte sheep retrovirus proviral sequences in the sheep genome. J. Virol. 77, 9662–9668 (2003)
Waugh O'Neill, R. J., O'Neill, M. J. & Graves, J. A. Undermethylation associated with retroelement activation and chromosome remodelling in an interspecific mammalian hybrid. Nature 396, 68–72 (1998)
Delassus, S., Sonigo, P. & Wain-Hobson, S. Genetic organisation of gibbon ape leukemia virus. Virology 173, 205–213 (1989)
Battini, J., Heard, J. M. & Danos, O. Receptor choice determinants in the envelope glycoproteins of amphotropic, xenotropic, and polytropic murine leukemia viruses. J. Virol. 66, 1468–1475 (1992)
Tailor, A. K. & Willet, B. J. in The 15th International Workshop on Retroviral Pathogenesis abstr. B.5 (Glasgow, Scotland, 2003).
Fauci, A. S. & Desrosiers, R. C. in Retroviruses (eds Coffin, J. M., Hughes, S. H. & Varmus, H. E.) 587–636 (Cold Spring Harbor Laboratory Press, New York, 1997)
Belshaw, R. et al. Long-term reinfection of the human genome by endogenous retroviruses. Proc. Natl Acad. Sci. USA 101, 4894–4899 (2004)
Martin, R. & Handasyde, K. in Managing Koalas in New South Wales: Proceedings of the Koala Summit held at the University of Sydney 7–8 November 1988 (eds Lunney, D., Urquhart, C. A. & Reed, P.) 58–66 (NSW National Parks and Wildlife Service, Sydney, 1990)
Masters, P., Duka, T., Berris, S. & Moss, G. Koalas on Kangaroo Island: from introduction to pest status in less than a century. Wildl. Res. 31, 267–272 (2004)
Bromham, L. The human zoo: endogenous retroviruses in the human genome. Trends Ecol. Evol. 17, 91–97 (2002)
Mang, R., Maas, J., Chen, X., Goudsmit, J. & Van der Kuyl, A. Identification of a novel type C porcine endogenous retrovirus: evidence that copy number of endogenous retroviruses increases during host inbreeding. J. Gen. Virol. 82, 1829–1834 (2001)
Jaenisch, R. Germ line integration and Mendelian transmission of the exogenous Moloney leukemia virus. Proc. Natl Acad. Sci. USA 73, 1260–1264 (1976)
Frankel, W. N., Stoye, J. P., Taylor, B. A. & Coffin, J. M. Genetic identification of endogenous polytropic proviruses by using recombinant inbred mice. J. Virol. 63, 3810–3821 (1989)
Steffen, D. L., Taylor, B. A. & Weinberg, R. A. Continuing germ line integration of AKC proviruses during the breeding of AKR mice and derivative recombinant inbred strains. J. Virol. 42, 165–175 (1982)
Sharp, A. The Koala Book (David Bateman, Auckland, 1995)
We thank J. Hanger, J. McKee, D. Hume and M. Eiden for discussions; Dreamworld Themepark, Queensland Parks and Wildlife Service, The South Australian Department of the Environment and Heritage, D. Higgins, S. Johnston and W. Ellis for access to, and supply of, samples; D. Irwin and staff at the Australian Genome and Research Facility for technical assistance with the single-cell PCR; B. Carroll and staff in the School of Molecular and Microbial Sciences, University of Queensland, for technical assistance with the Southern blotting analyses. This work was supported by Dreamworld Themepark and the Australian Research Council. Author Contributions R.E.T. carried out all experiments shown in Figs 1–3 and in Supplementary Information. All authors were involved in the conceptual design and interpretation of the experimental work with direction and supervision provided by J.M. and P.R.Y. All authors participated in the drafting of the manuscript.
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
About this article
Cite this article
Tarlinton, R., Meers, J. & Young, P. Retroviral invasion of the koala genome. Nature 442, 79–81 (2006). https://doi.org/10.1038/nature04841
Genome Biology (2021)
Genome Biology (2021)
Nature Communications (2021)
Nature Reviews Genetics (2021)
Archives of Virology (2021)