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

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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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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.",
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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 journalArticleResearchpeer-review

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AU - Benavente, Ernest Diez

AU - Gomes, Ana Rita

AU - De Silva, Jeremy Ryan

AU - Grigg, Matthew

AU - Walker, Harriet

AU - Barber, Bridget E.

AU - William, Timothy

AU - Yeo, Tsin Wen

AU - de Sessions, Paola Florez

AU - Ramaprasad, Abhinay

AU - Ibrahim, Amy

AU - Charleston, James

AU - Hibberd, Martin L.

AU - Pain, Arnab

AU - Moon, Robert W.

AU - Auburn, Sarah

AU - Ling, Lau Yee

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AU - Clark, Taane G.

AU - Campino, Susana

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N2 - 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.

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