Whole genome sequencing of amplified Plasmodium knowlesi DNA from unprocessed blood reveals genetic exchange events between Malaysian Peninsular and Borneo subpopulations

Ernest Diez Benavente, Ana Rita Gomes, Jeremy Ryan De Silva, Matthew Grigg, Harriet Walker, Bridget E. Barber, Timothy William, Tsin Wen Yeo, Paola Florez de Sessions, Abhinay Ramaprasad, Amy Ibrahim, James Charleston, Martin L. Hibberd, Arnab Pain, Robert W. Moon, Sarah Auburn, Lau Yee Ling, Nicholas M. Anstey, Taane G. Clark, Susana Campino

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    Abstract

    The zoonotic Plasmodium knowlesi parasite is the most common cause of human malaria in Malaysia. Genetic analysis has shown that the parasites are divided into three subpopulations according to their geographic origin (Peninsular or Borneo) and, in Borneo, their macaque host (Macaca fascicularis or M. nemestrina). Whilst evidence suggests that genetic exchange events have occurred between the two Borneo subpopulations, the picture is unclear in less studied Peninsular strains. One difficulty is that P. knowlesi infected individuals tend to present with low parasitaemia leading to samples with insufficient DNA for whole genome sequencing. Here, using a parasite selective whole genome amplification approach on unprocessed blood samples, we were able to analyse recent genomes sourced from both Peninsular Malaysia and Borneo. The analysis provides evidence that recombination events are present in the Peninsular Malaysia parasite subpopulation, which have acquired fragments of the M. nemestrina associated subpopulation genotype, including the DBPβ and NBPXa erythrocyte invasion genes. The NBPXb invasion gene has also been exchanged within the macaque host-associated subpopulations of Malaysian Borneo. Our work provides strong evidence that exchange events are far more ubiquitous than expected and should be taken into consideration when studying the highly complex P. knowlesi population structure.

    Original languageEnglish
    Article number9873
    Pages (from-to)1-11
    Number of pages11
    JournalScientific Reports
    Volume9
    Issue number1
    Early online date8 Jul 2019
    DOIs
    Publication statusPublished - 1 Dec 2019

    Fingerprint

    Borneo
    Plasmodium knowlesi
    Genome
    Malaysia
    Parasites
    DNA
    Macaca
    Macaca fascicularis
    Parasitemia
    Zoonoses
    Genetic Recombination
    Genes
    Malaria
    Erythrocytes
    Genotype
    Population

    Cite this

    Benavente, Ernest Diez ; Gomes, Ana Rita ; De Silva, Jeremy Ryan ; Grigg, Matthew ; Walker, Harriet ; Barber, Bridget E. ; William, Timothy ; Yeo, Tsin Wen ; de Sessions, Paola Florez ; Ramaprasad, Abhinay ; Ibrahim, Amy ; Charleston, James ; Hibberd, Martin L. ; Pain, Arnab ; Moon, Robert W. ; Auburn, Sarah ; Ling, Lau Yee ; Anstey, Nicholas M. ; Clark, Taane G. ; Campino, Susana. / Whole genome sequencing of amplified Plasmodium knowlesi DNA from unprocessed blood reveals genetic exchange events between Malaysian Peninsular and Borneo subpopulations. In: Scientific Reports. 2019 ; Vol. 9, No. 1. pp. 1-11.
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    title = "Whole genome sequencing of amplified Plasmodium knowlesi DNA from unprocessed blood reveals genetic exchange events between Malaysian Peninsular and Borneo subpopulations",
    abstract = "The zoonotic Plasmodium knowlesi parasite is the most common cause of human malaria in Malaysia. Genetic analysis has shown that the parasites are divided into three subpopulations according to their geographic origin (Peninsular or Borneo) and, in Borneo, their macaque host (Macaca fascicularis or M. nemestrina). Whilst evidence suggests that genetic exchange events have occurred between the two Borneo subpopulations, the picture is unclear in less studied Peninsular strains. One difficulty is that P. knowlesi infected individuals tend to present with low parasitaemia leading to samples with insufficient DNA for whole genome sequencing. Here, using a parasite selective whole genome amplification approach on unprocessed blood samples, we were able to analyse recent genomes sourced from both Peninsular Malaysia and Borneo. The analysis provides evidence that recombination events are present in the Peninsular Malaysia parasite subpopulation, which have acquired fragments of the M. nemestrina associated subpopulation genotype, including the DBPβ and NBPXa erythrocyte invasion genes. The NBPXb invasion gene has also been exchanged within the macaque host-associated subpopulations of Malaysian Borneo. Our work provides strong evidence that exchange events are far more ubiquitous than expected and should be taken into consideration when studying the highly complex P. knowlesi population structure.",
    author = "Benavente, {Ernest Diez} and Gomes, {Ana Rita} and {De Silva}, {Jeremy Ryan} and Matthew Grigg and Harriet Walker and Barber, {Bridget E.} and Timothy William and Yeo, {Tsin Wen} and {de Sessions}, {Paola Florez} and Abhinay Ramaprasad and Amy Ibrahim and James Charleston and Hibberd, {Martin L.} and Arnab Pain and Moon, {Robert W.} and Sarah Auburn and Ling, {Lau Yee} and Anstey, {Nicholas M.} and Clark, {Taane G.} and Susana Campino",
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    Benavente, ED, Gomes, AR, De Silva, JR, Grigg, M, Walker, H, Barber, BE, William, T, Yeo, TW, de Sessions, PF, Ramaprasad, A, Ibrahim, A, Charleston, J, Hibberd, ML, Pain, A, Moon, RW, Auburn, S, Ling, LY, Anstey, NM, Clark, TG & Campino, S 2019, 'Whole genome sequencing of amplified Plasmodium knowlesi DNA from unprocessed blood reveals genetic exchange events between Malaysian Peninsular and Borneo subpopulations', Scientific Reports, vol. 9, no. 1, 9873, pp. 1-11. https://doi.org/10.1038/s41598-019-46398-z

    Whole genome sequencing of amplified Plasmodium knowlesi DNA from unprocessed blood reveals genetic exchange events between Malaysian Peninsular and Borneo subpopulations. / Benavente, Ernest Diez; Gomes, Ana Rita; De Silva, Jeremy Ryan; Grigg, Matthew; Walker, Harriet; Barber, Bridget E.; William, Timothy; Yeo, Tsin Wen; de Sessions, Paola Florez; Ramaprasad, Abhinay; Ibrahim, Amy; Charleston, James; Hibberd, Martin L.; Pain, Arnab; Moon, Robert W.; Auburn, Sarah; Ling, Lau Yee; Anstey, Nicholas M.; Clark, Taane G.; Campino, Susana.

    In: Scientific Reports, Vol. 9, No. 1, 9873, 01.12.2019, p. 1-11.

    Research output: Contribution to journalArticle

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    AU - Charleston, James

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    AU - Pain, Arnab

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    AU - Auburn, Sarah

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