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Genetic Diversity and Evolution

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

Niccolò Alfano, Johan Michaux, Serge Morand, Ken Aplin, Kyriakos Tsangaras, Ulrike Löber, Pierre-Henri Fabre, Yuli Fitriana, Gono Semiadi, Yasuko Ishida, Kristofer M. Helgen, Alfred L. Roca, Maribeth V. Eiden, Alex D. Greenwood
K. L. Beemon, Editor
Niccolò Alfano
aLeibniz Institute for Zoo and Wildlife Research, Berlin, Germany
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Johan Michaux
bConservation Genetics Unit, Institute of Botany, University of Liège, Liège, Belgium
cCIRAD, Campus international de Baillarguet, Montpellier, France
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Serge Morand
dCIRAD-CNRS, Centre d'Infectiologie Christophe Mérieux du Laos, Vientiane, Lao PDR
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Ken Aplin
eNational Museum of Natural History, Smithsonian Institution, Washington, DC, USA
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Kyriakos Tsangaras
aLeibniz Institute for Zoo and Wildlife Research, Berlin, Germany
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Ulrike Löber
aLeibniz Institute for Zoo and Wildlife Research, Berlin, Germany
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Pierre-Henri Fabre
eNational Museum of Natural History, Smithsonian Institution, Washington, DC, USA
fInstitut des Sciences de l'Evolution de Montpellier (ISEM-UMR 5554 UM2-CNRS-IRD), Montpellier University, Montpellier, France
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Yuli Fitriana
gMuseum Zoologicum Bogoriense, Research Center For Biology, Indonesian Institute of Sciences (LIPI), Cibinong, Indonesia
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Gono Semiadi
gMuseum Zoologicum Bogoriense, Research Center For Biology, Indonesian Institute of Sciences (LIPI), Cibinong, Indonesia
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Yasuko Ishida
hDepartment of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA
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Kristofer M. Helgen
eNational Museum of Natural History, Smithsonian Institution, Washington, DC, USA
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Alfred L. Roca
hDepartment of Animal Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois, USA
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Maribeth V. Eiden
iSection on Directed Gene Transfer, Laboratory of Cellular and Molecular Regulation, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland, USA
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Alex D. Greenwood
aLeibniz Institute for Zoo and Wildlife Research, Berlin, Germany
jDepartment of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany
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K. L. Beemon
Johns Hopkins University
Roles: Editor
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DOI: 10.1128/JVI.00723-16
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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.

FOOTNOTES

    • Received 27 April 2016.
    • Accepted 27 June 2016.
    • Accepted manuscript posted online 6 July 2016.
  • Address correspondence to Alex D. Greenwood, greenwood{at}izw-berlin.de.
  • ↵* Present address: Kyriakos Tsangaras, Cyprus Institute of Neurology and Genetics, Nicosia, Cyprus.

  • Citation Alfano N, Michaux J, Morand S, Aplin K, Tsangaras K, Löber U, Fabre P-H, Fitriana Y, Semiadi G, Ishida Y, Helgen KM, Roca AL, Eiden MV, Greenwood AD. 2016. Endogenous gibbon ape leukemia virus identified in a rodent (Melomys burtoni subsp.) from Wallacea (Indonesia). J Virol 90:8169–8180. doi:10.1128/JVI.00723-16.

  • Copyright © 2016, American Society for Microbiology. All Rights Reserved.
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Endogenous Gibbon Ape Leukemia Virus Identified in a Rodent (Melomys burtoni subsp.) from Wallacea (Indonesia)
Niccolò Alfano, Johan Michaux, Serge Morand, Ken Aplin, Kyriakos Tsangaras, Ulrike Löber, Pierre-Henri Fabre, Yuli Fitriana, Gono Semiadi, Yasuko Ishida, Kristofer M. Helgen, Alfred L. Roca, Maribeth V. Eiden, Alex D. Greenwood
Journal of Virology Aug 2016, 90 (18) 8169-8180; DOI: 10.1128/JVI.00723-16

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Endogenous Gibbon Ape Leukemia Virus Identified in a Rodent (Melomys burtoni subsp.) from Wallacea (Indonesia)
Niccolò Alfano, Johan Michaux, Serge Morand, Ken Aplin, Kyriakos Tsangaras, Ulrike Löber, Pierre-Henri Fabre, Yuli Fitriana, Gono Semiadi, Yasuko Ishida, Kristofer M. Helgen, Alfred L. Roca, Maribeth V. Eiden, Alex D. Greenwood
Journal of Virology Aug 2016, 90 (18) 8169-8180; DOI: 10.1128/JVI.00723-16
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