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

Handle URI:
http://hdl.handle.net/10754/625486
Title:
Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations
Authors:
Diez Benavente, Ernest; Florez de Sessions, Paola; Moon, Robert W. ( 0000-0002-9070-4292 ) ; Holder, Anthony A. ( 0000-0002-8490-6058 ) ; Blackman, Michael J. ( 0000-0002-7442-3810 ) ; Roper, Cally ( 0000-0002-6545-309X ) ; Drakeley, Christopher J.; Pain, Arnab ( 0000-0002-1755-2819 ) ; Sutherland, Colin J.; Hibberd, Martin L. ( 0000-0001-8587-1849 ) ; Campino, Susana; Clark, Taane G. ( 0000-0001-8985-9265 )
Abstract:
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.
KAUST Department:
King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia.
Citation:
Diez Benavente E, Florez de Sessions P, Moon RW, Holder AA, Blackman MJ, et al. (2017) Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations. PLOS Genetics 13: e1007008. Available: http://dx.doi.org/10.1371/journal.pgen.1007008.
Publisher:
Public Library of Science (PLoS)
Journal:
PLOS Genetics
Issue Date:
18-Sep-2017
DOI:
10.1371/journal.pgen.1007008
Type:
Article
ISSN:
1553-7404
Sponsors:
TGC is funded by the Medical Research Council UK (Grant no. MR/K000551/1, MR/M01360X/1, MR/N010469/1, MC_PC_15103). SC and CR are funded by the Medical Research Council UK (Grant no. MR/M01360X/1). RWM is supported by an MRC Career Development Award jointly funded by the UK MRC and UK Department for International Development. This work was supported in part by the Francis Crick Institute that receives its core funding from Cancer Research UK (FC001097, FC001043), the UK Medical Research Council (FC001097, FC001043), and the Wellcome Trust (FC001097, FC001043). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Additional Links:
http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1007008
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Articles

Full metadata record

DC FieldValue Language
dc.contributor.authorDiez Benavente, Ernesten
dc.contributor.authorFlorez de Sessions, Paolaen
dc.contributor.authorMoon, Robert W.en
dc.contributor.authorHolder, Anthony A.en
dc.contributor.authorBlackman, Michael J.en
dc.contributor.authorRoper, Callyen
dc.contributor.authorDrakeley, Christopher J.en
dc.contributor.authorPain, Arnaben
dc.contributor.authorSutherland, Colin J.en
dc.contributor.authorHibberd, Martin L.en
dc.contributor.authorCampino, Susanaen
dc.contributor.authorClark, Taane G.en
dc.date.accessioned2017-09-21T09:12:12Z-
dc.date.available2017-09-21T09:12:12Z-
dc.date.issued2017-09-18en
dc.identifier.citationDiez Benavente E, Florez de Sessions P, Moon RW, Holder AA, Blackman MJ, et al. (2017) Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations. PLOS Genetics 13: e1007008. Available: http://dx.doi.org/10.1371/journal.pgen.1007008.en
dc.identifier.issn1553-7404en
dc.identifier.doi10.1371/journal.pgen.1007008en
dc.identifier.urihttp://hdl.handle.net/10754/625486-
dc.description.abstractThe 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.en
dc.description.sponsorshipTGC is funded by the Medical Research Council UK (Grant no. MR/K000551/1, MR/M01360X/1, MR/N010469/1, MC_PC_15103). SC and CR are funded by the Medical Research Council UK (Grant no. MR/M01360X/1). RWM is supported by an MRC Career Development Award jointly funded by the UK MRC and UK Department for International Development. This work was supported in part by the Francis Crick Institute that receives its core funding from Cancer Research UK (FC001097, FC001043), the UK Medical Research Council (FC001097, FC001043), and the Wellcome Trust (FC001097, FC001043). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.en
dc.publisherPublic Library of Science (PLoS)en
dc.relation.urlhttp://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1007008en
dc.rightsThis is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.titleAnalysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulationsen
dc.typeArticleen
dc.contributor.departmentKing Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia.en
dc.identifier.journalPLOS Geneticsen
dc.eprint.versionPost-printen
dc.contributor.institutionFaculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom.en
dc.contributor.institutionGenome Institute of Singapore, Biopolis, Singapore.en
dc.contributor.institutionThe Francis Crick Institute, London, United Kingdom.en
kaust.authorPain, Arnaben
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