African Non-Human Primates Host Diverse Enteroviruses

Abstract

Enteroviruses (EVs) belong to the family Picornaviridae and are responsible for mild to severe diseases in mammals including humans and non-human primates (NHP). Simian EVs were first discovered in the 1950s in the Old World Monkeys and recently in wild chimpanzee, gorilla and mandrill in Cameroon. In the present study, we screened by PCR EVs in 600 fecal samples of wild apes and monkeys that were collected at four sites in Gabon. A total of 32 samples were positive for EVs (25 from mandrills, 7 from chimpanzees, none from gorillas). The phylogenetic analysis of VP1 and VP2 genes showed that EVs identified in chimpanzees were members of two human EV species, EV-A and EV-B, and those identified in mandrills were members of the human species EV-B and the simian species EV-J. The identification of two novel enterovirus types, EV-B112 in a chimpanzee and EV-B113 in a mandrill, suggests these NHPs could be potential sources of new EV types. The identification of EV-B107 and EV90 that were previously found in humans indicates cross-species transfers. Also the identification of chimpanzee-derived EV110 in a mandrill demonstrated a wide host range of this EV. Further research of EVs in NHPs would help understanding emergence of new types or variants, and evaluating the real risk of cross-species transmission for humans as well for NHPs populations.

Fig 1. Non-human primates sampling sites in Gabon.

For each site, the zone code is indicated: IV for Ivindo, LE for Lékédi, LO for Lopé, MI for Mikongo. The circles indicate positive EV samples detected in this study; numbers inside circles indicate the number of positive EV samples. Host species that yielded EVs are indicated in blue for chimpanzee and green for mandrills.

Fig 2. Phylogenetic relationship of EV strains based on approximately 450 nucleotides VP2 sequences (positions 962 to 1,545 according to the poliovirus 1 genome, Genbank # V01149), in the species EV-B, EV-A and EV-J.

The genus tree was constructed using the partial VP2 sequences of representative serotypes of the genus Enterovirus by maximum likelihood method. Sequences obtained in this study are indicated in blue for mandrills and green for chimpanzees. Reference EV sequences of other NHP species are indicated in red. Names of NHP species are indicated (Mac for macaque, Bab for baboon, Cer for cercopothecus), countries are also indicated (BAN, Bangladesh; CHN for China; CIV for Ivory Coast; CMR for Cameroon; FRA for France; JPN for Japan; KOR for South Korea; MEX for Mexico; NLD for Netherland; PHL for Philippines; PUR for Puerto Rico; SLN for Slovenia; USA for United States of America; and SOA for Republic of South Africa). Trees were built using Maximum likelihood algorithm and GTR substitution model. Only bootstrap values ≥ 60% are indicated at the nodes. Scale bars represent the genetic distance. GenBank accession numbers of the sequences used are indicated in the tree (for details, see S4 Table).

Fig 3. Phylogenetic relationship of EV strains based on approximately 320 nucleotides of the VP1 gene (positions 2,602 to 2,951 according to the poliovirus 1 genome, Genbank # V01149).

Methods and designations are identical to Fig 2.

Fig 4. Similarity plot and bootscanning analysis of samples GAB98, GAB130 and GAB653.

Similarity plot was performed using a sliding window of 400 nt moving with 20-nt step (800 nt window with 50-nt step for GAB653) and bootscanning was done using the Neighbor-joining method. The genome structure is indicated above the plot.

Fig 5

Phylogenetic relationship of human and NHP EV-B based on the complete 2C gene (a) and 935 nucleotides of the 3D region, from position 5,979 to 6,914 of the PV1 Mahoney strain (GenBank #V01149) (b). Designations are identical to Fig 2.