Widespread Infection with Homologues of Human Parvoviruses B19, PARV4, and Human Bocavirus of Chimpanzees and Gorillas in the Wild

Author:

Sharp Colin P.1,LeBreton Matthew2,Kantola Kalle3,Nana Ahmadou2,Diffo Joseph Le Doux2,Djoko Cyrille F.2,Tamoufe Ubald2,Kiyang John A.4,Babila Tafon G.5,Ngole Eitel Mpoudi6,Pybus Oliver G.7,Delwart Eric8,Delaporte Eric9,Peeters Martine9,Soderlund-Venermo Maria3,Hedman Klaus310,Wolfe Nathan D.211,Simmonds Peter1

Affiliation:

1. Centre for Infectious Diseases, University of Edinburgh, Summerhall, Edinburgh EH9 1QH, Scotland

2. Global Viral Forecasting, One Sutter, Suite 600, San Francisco, California 94101

3. Helsinki University Central Hospital Laboratory Division, Helsinki, Finland

4. Limbe Wildlife Centre, BP 878, Limbe, Cameroon

5. Ape Action Africa, BP 20072, Yaounde, Cameroon

6. Projet Prevention du Sida ou Cameroun (PRESICA), Yaoundé, Cameroon

7. Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom

8. Blood Systems Research Institute and Department of Laboratory Medicine, University of California—San Francisco, San Francisco, California 94118

9. UMR145, Institut de Recherche pour le Développement and Department of International Health, University of Montpellier 1, 34394 Montpellier Cedex 5, France

10. Department of Virology, Haartman Institute, University of Helsinki, Helsinki, Finland

11. Department of Human Biology, Stanford University, Stanford, California

Abstract

ABSTRACT Infections with human parvoviruses B19 and recently discovered human bocaviruses (HBoVs) are widespread, while PARV4 infections are transmitted parenterally and prevalent specifically in injecting drug users and hemophiliacs. To investigate the exposure and circulation of parvoviruses related to B19 virus, PARV4, and HBoV in nonhuman primates, plasma samples collected from 73 Cameroonian wild-caught chimpanzees and gorillas and 91 Old World monkey (OWM) species were screened for antibodies to recombinant B19 virus, PARV4, and HBoV VP2 antigens by enzyme-linked immunosorbent assay (ELISA). Moderate to high frequencies of seroreactivity to PARV4 (63% and 18% in chimpanzees and gorillas, respectively), HBoV (73% and 36%), and B19 virus (8% and 27%) were recorded for apes, while OWMs were uniformly negative (for PARV4 and B19 virus) or infrequently reactive (3% for HBoV). For genetic characterization, plasma samples and 54 fecal samples from chimpanzees and gorillas collected from Cameroonian forest floors were screened by PCR with primers conserved within Erythrovirus , Bocavirus , and PARV4 genera. Two plasma samples (chimpanzee and baboon) were positive for PARV4, while four fecal samples were positive for HBoV-like viruses. The chimpanzee PARV4 variant showed 18% and 15% nucleotide sequence divergence in NS and VP1/2, respectively, from human variants (9% and 7% amino acid, respectively), while the baboon variant was substantially more divergent, mirroring host phylogeny. Ape HBoV variants showed complex sequence relationships with human viruses, comprising separate divergent homologues of HBoV1 and the recombinant HBoV3 species in chimpanzees and a novel recombinant species in gorillas. This study provides the first evidence for widespread circulation of parvoviruses in primates and enables future investigations of their epidemiology, host specificity, and (co)evolutionary histories.

Publisher

American Society for Microbiology

Subject

Virology,Insect Science,Immunology,Microbiology

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