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

Ernest Diez Benavente; Paola Florez de Sessions; Robert W. Moon; Anthony A. Holder; Michael J. Blackman; Cally Roper; Christopher J. Drakeley; Arnab Pain; Colin J. Sutherland; Martin L. Hibberd; Susana Campino; Taane G. Clark

doi:10.1371/journal.pgen.1007008

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

Ernest Diez Benavente, Paola Florez de Sessions, Robert W. Moon, Anthony A. Holder, Michael J. Blackman, Cally Roper, Christopher J. Drakeley, Arnab Pain, Colin J. Sutherland, Martin L. Hibberd, Susana Campino, Taane G. Clark

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18 Scopus citations

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.

Original language	English (US)
Pages (from-to)	e1007008
Journal	PLOS Genetics
Volume	13
Issue number	9
DOIs	https://doi.org/10.1371/journal.pgen.1007008
State	Published - Sep 18 2017

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: 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.

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https://repository.kaust.edu.sa/bitstream/10754/625486/1/journal.pgen.1007008.pdf

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Diez Benavente, E., Florez de Sessions, P., Moon, R. W., Holder, A. A., Blackman, M. J., Roper, C., Drakeley, C. J., Pain, A., Sutherland, C. J., Hibberd, M. L., Campino, S., & Clark, T. G. (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(9), e1007008. https://doi.org/10.1371/journal.pgen.1007008

@article{678d809ba2064d1796249422247c4e05,

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

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.",

author = "{Diez Benavente}, Ernest and {Florez de Sessions}, Paola and Moon, {Robert W.} and Holder, {Anthony A.} and Blackman, {Michael J.} and Cally Roper and Drakeley, {Christopher J.} and Arnab Pain and Sutherland, {Colin J.} and Hibberd, {Martin L.} and Susana Campino and Clark, {Taane G.}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: 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.",

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Diez Benavente, E, Florez de Sessions, P, Moon, RW, Holder, AA, Blackman, MJ, Roper, C, Drakeley, CJ, Pain, A, Sutherland, CJ, Hibberd, ML, Campino, S & Clark, TG 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, vol. 13, no. 9, pp. e1007008. https://doi.org/10.1371/journal.pgen.1007008

Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations. / Diez Benavente, Ernest; Florez de Sessions, Paola; Moon, Robert W. et al.
In: PLOS Genetics, Vol. 13, No. 9, 18.09.2017, p. e1007008.

Research output: Contribution to journal › Article › peer-review

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T1 - Analysis of nuclear and organellar genomes of Plasmodium knowlesi in humans reveals ancient population structure and recent recombination among host-specific subpopulations

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AU - Florez de Sessions, Paola

AU - Moon, Robert W.

AU - Holder, Anthony A.

AU - Blackman, Michael J.

AU - Roper, Cally

AU - Drakeley, Christopher J.

AU - Pain, Arnab

AU - Sutherland, Colin J.

AU - Hibberd, Martin L.

AU - Campino, Susana

AU - Clark, Taane G.

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: 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.

PY - 2017/9/18

Y1 - 2017/9/18

N2 - 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.

AB - 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.

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JF - PLOS Genetics

IS - 9

ER -

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

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