Isolates of Zaire ebolavirus from wild apes reveal genetic lineage and recombinants

Abstract

Over the last 30 years, Zaire ebolavirus (ZEBOV), a virus highly pathogenic for humans and wild apes, has emerged repeatedly in Central Africa. Thus far, only a few virus isolates have been characterized genetically, all belonging to a single genetic lineage and originating exclusively from infected human patients. Here, we describe the first ZEBOV sequences isolated from great ape carcasses in the Gabon/Congo region that belong to a previously unrecognized genetic lineage. According to our estimates, this lineage, which we also encountered in the two most recent human outbreaks in the Republic of the Congo in 2003 and 2005, diverged from the previously known viruses around the time of the first documented human outbreak in 1976. These results suggest that virus spillover from the reservoir has occurred more than once, as predicted by the multiple emergence hypothesis. However, the young age of both ZEBOV lineages and the spatial and temporal sequence of outbreaks remain at odds with the idea that the virus simply emerged from a long-established and widespread reservoir population. Based on data from two ZEBOV genes, we also demonstrate, within the family Filoviridae, recombination between the two lineages. According to our estimates, this event took place between 1996 and 2001 and gave rise to a group of recombinant viruses that were responsible for a series of outbreaks in 2001-2003. The potential for recombination adds an additional level of complexity to unraveling and potentially controlling the emergence of ZEBOV in humans and wildlife species.

Fig. 1.

Phylogenetic trees inferred from GP gene (A) and NP gene (B) sequences that show relationships among all of the ZEBOV isolates. Viruses derived from wild ape carcasses are shown in bold. Values above branches represent Bayesian posterior probabilities and ML bootstrap scores (both as percentages). Colors identify three genetic groups of ZEBOV: green, group A; red, group B; blue, recombinant group R.

Fig. 2.

Timing and longitudinal location of all ZEBOV outbreaks from 2001 onward that were included in the phylogenetic analysis. Blue and red symbols indicate outbreaks caused by group B and group R viruses, respectively. Squares, human outbreaks; circles, ape carcasses.

Fig. 3.

Location of sources of all ZEBOV isolates genetically identified in humans and great apes from the first 1976 outbreak to the present. The source (GOR, gorilla; CH, chimpanzee), location, and month of sampling are specified. Colors relect virus groups (Fig. 1).