Endogenous Gibbon Ape Leukemia Virus Identified in a Rodent (Melomys burtoni subsp.) from Wallacea (Indonesia)

Author:

Alfano Niccolò1,Michaux Johan23,Morand Serge4,Aplin Ken5,Tsangaras Kyriakos1,Löber Ulrike1,Fabre Pierre-Henri56,Fitriana Yuli7,Semiadi Gono7,Ishida Yasuko8,Helgen Kristofer M.5,Roca Alfred L.8,Eiden Maribeth V.9,Greenwood Alex D.110

Affiliation:

1. Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany

2. Conservation Genetics Unit, Institute of Botany, University of Liège, Liège, Belgium

3. CIRAD, Campus international de Baillarguet, Montpellier, France

4. CIRAD-CNRS, Centre d'Infectiologie Christophe Mérieux du Laos, Vientiane, Lao PDR

5. National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

6. Institut des Sciences de l'Evolution de Montpellier (ISEM-UMR 5554 UM2-CNRS-IRD), Montpellier University, Montpellier, France

7. Museum Zoologicum Bogoriense, Research Center For Biology, Indonesian Institute of Sciences (LIPI), Cibinong, Indonesia

8. Department of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA

9. Section on Directed Gene Transfer, Laboratory of Cellular and Molecular Regulation, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland, USA

10. Department of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany

Abstract

ABSTRACT Gibbon ape leukemia virus (GALV) and koala retrovirus (KoRV) most likely originated from a cross-species transmission of an ancestral retrovirus into koalas and gibbons via one or more intermediate as-yet-unknown hosts. A virus highly similar to GALV has been identified in an Australian native rodent ( Melomys burtoni ) after extensive screening of Australian wildlife. GALV-like viruses have also been discovered in several Southeast Asian species, although screening has not been extensive and viruses discovered to date are only distantly related to GALV. We therefore screened 26 Southeast Asian rodent species for KoRV- and GALV-like sequences, using hybridization capture and high-throughput sequencing, in the attempt to identify potential GALV and KoRV hosts. Only the individuals belonging to a newly discovered subspecies of Melomys burtoni from Indonesia were positive, yielding an endogenous provirus very closely related to a strain of GALV. The sequence of the critical receptor domain for GALV infection in the Indonesian M. burtoni subsp. was consistent with the susceptibility of the species to GALV infection. The second record of a GALV in M. burtoni provides further evidence that M. burtoni , and potentially other lineages within the widespread subfamily Murinae , may play a role in the spread of GALV-like viruses. The discovery of a GALV in the most western part of the Australo-Papuan distribution of M. burtoni , specifically in a transitional zone between Asia and Australia (Wallacea), may be relevant to the cross-species transmission to gibbons in Southeast Asia and broadens the known distribution of GALVs in wild rodents. IMPORTANCE Gibbon ape leukemia virus (GALV) and the koala retrovirus (KoRV) are very closely related, yet their hosts neither are closely related nor overlap geographically. Direct cross-species infection between koalas and gibbons is unlikely. Therefore, GALV and KoRV may have arisen via a cross-species transfer from an intermediate host whose range overlaps those of both gibbons and koalas. Using hybridization capture and high-throughput sequencing, we have screened a wide range of rodent candidate hosts from Southeast Asia for KoRV- and GALV-like sequences. Only a Melomys burtoni subspecies from Wallacea (Indonesia) was positive for GALV. We report the genome sequence of this newly identified GALV, the critical domain for infection of its potential cellular receptor, and its phylogenetic relationships with the other previously characterized GALVs. We hypothesize that Melomys burtoni , and potentially related lineages with an Australo-Papuan distribution, may have played a key role in cross-species transmission to other taxa.

Publisher

American Society for Microbiology

Subject

Virology,Insect Science,Immunology,Microbiology

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1. A recent gibbon ape leukemia virus germline integration in a rodent from New Guinea;Proceedings of the National Academy of Sciences;2024-02

2. Wildlife endogenous retroviruses: colonization, consequences, and cooption;Trends in Genetics;2023-11

3. Nonhuman primate (NHP) species from India and Africa;Global Perspectives on the Transmission of Zoonotic RNA Viruses from Wild Animal Species to Humans;2023

4. Metatranscriptomics Analysis Reveals Diverse Viral RNA in Cutaneous Papillomatous Lesions of Cattle;Evolutionary Bioinformatics;2022-01

5. Retroviruses of Bats: a Threat Waiting in the Wings?;mBio;2021-10-26

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