Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations

• Published in: PLoS genetics 2017-09, Vol.13 (9), p.e1007008-e1007008
• Main Authors: Diez Benavente, Ernest, Florez de Sessions, Paola, Moon, Robert W, Holder, Anthony A, Blackman, Michael J, Roper, Cally, Drakeley, Christopher J, Pain, Arnab, Sutherland, Colin J, Hibberd, Martin L, Campino, Susana, Clark, Taane G
• Format: Article
• Language: English
• Subjects: Animals; Bioinformatics; Biology and life sciences; Chromosome 8; Computer and Information Sciences; Councils; Crick, Francis; Culicidae - genetics; Culicidae - parasitology; Deforestation; Dimorphism; Epidemiology; Evolution; Funding; Genetic aspects; Genetic recombination; Genetics; Genome; Genomes; Genotypes; Health aspects; Host-parasite relationships; Host-Pathogen Interactions - genetics; Humans; Hygiene; Infections; Insect Vectors - genetics; Macaca fascicularis; Macaca fascicularis - genetics; Macaca fascicularis - parasitology; Macaca nemestrina; Macaca nemestrina - genetics; Macaca nemestrina - parasitology; Macaques; Malaria; Malaria - genetics; Malaria - parasitology; Malaria - transmission; Manganese; Medical research; Medicine; Medicine and Health Sciences; Mosaics; Organelles - genetics; Organelles - parasitology; Parameter estimation; Parasites; Phylogenetics; Plasmodium; Plasmodium (Protozoa); Plasmodium falciparum; Plasmodium knowlesi; Plasmodium knowlesi - genetics; Plasmodium knowlesi - pathogenicity; Plasmodium ovale; Population; Population structure; Recombination; Subpopulations; Supervision; Tropical diseases
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1007008

The macaque parasite Plasmodium knowlesi is a significant concern in Malaysia where cases of human infection are increasing. Parasites infecting humans originate from genetically distinct subpopulations associated with the long-tailed (Macaca fascicularis (Mf)) or pig-tailed macaques (Macaca nemestrina (Mn)). We used a new high-quality reference genome to re-evaluate previously described subpopulations among human and macaque isolates from Malaysian-Borneo and Peninsular-Malaysia. Nuclear genomes were dimorphic, as expected, but new evidence of chromosomal-segment exchanges between subpopulations was found. A large segment on chromosome 8 originating from the Mn subpopulation and containing genes encoding proteins expressed in mosquito-borne parasite stages, was found in Mf genotypes. By contrast, non-recombining organelle genomes partitioned into 3 deeply branched lineages, unlinked with nuclear genomic dimorphism. Subpopulations which diverged in isolation have re-connected, possibly due to deforestation and disruption of wild macaque habitats. The resulting genomic mosaics reveal traits selected by host-vector-parasite interactions in a setting of ecological transition.