Widespread infection with homologues of human parvoviruses B19, PARV4, and human bocavirus of chimpanzees and gorillas in the wild

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.

FIG. 1.

Frequency of serological reactivity of chimpanzee, gorilla, and OWP plasma samples in B19 virus, PARV4, and HBoV antibody ELISAs (number positive/number tested shown above each bar).

FIG. 2.

Phylogenetic analysis of (A) complete NS and (B) VP1/VP2 gene sequences and (C) partial VP2 sequence (positions 3067 to 3310) of the chimpanzee and baboon variants (PT-P48 and PA-P68; solid circles) and available complete genome sequences of PARV4 genotypes (Gt) 1 to 3 and of porcine and bovine homologues (PHoV, BHoV). Different species and genotypes are represented with different symbols and shading. PARV4 sequences showing <0.5% divergence from other sequences were excluded from analysis. The trees were constructed by neighbor joining of pairwise Jukes-Cantor corrected distances between nucleotide sequences; bootstrap values of ≥70% are shown.

FIG. 3.

Phylogenetic analysis of partial NS (positions 1096 to 1581) and VP1/VP2 (positions 4343 to 4828) gene sequences of bocavirus-like sequences amplified from chimpanzee (prefixed PT) and gorilla (GG) positive fecal samples. Sequences were compared with available complete genome sequences of HBoV1-HBoV4 and the more divergent canine (MVC) and bovine (BPV-1) members of the Bocavirus genus. Different species and genotypes are represented with different symbols and shading. HBoV1 and HBoV2 sequences showing <0.5% divergence from other sequences were excluded from analysis. The trees were constructed by neighbor joining of pairwise Jukes-Cantor corrected distances between nucleotide sequences; bootstrap values of ≥70% are shown.