Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.

Sabah, Malaysia, has amongst the highest burden of human Plasmodium knowlesi infection in the world, associated with increasing encroachment on the parasite's macaque host habitat. However, the genomic make-up of P. knowlesi in Sabah was previously poorly understood. To inform on local patterns...

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Main Authors: Jacob A F Westaway, Ernest Diez Benavente, Sarah Auburn, Michal Kucharski, Nicolas Aranciaga, Sourav Nayak, Timothy William, Giri S Rajahram, Kim A Piera, Kamil Braima, Angelica F Tan, Danshy A Alaza, Bridget E Barber, Chris Drakeley, Roberto Amato, Edwin Sutanto, Hidayat Trimarsanto, Jenarun Jelip, Nicholas M Anstey, Zbynek Bozdech, Matthew Field, Matthew J Grigg
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-03-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://doi.org/10.1371/journal.pntd.0012885
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author Jacob A F Westaway
Ernest Diez Benavente
Sarah Auburn
Michal Kucharski
Nicolas Aranciaga
Sourav Nayak
Timothy William
Giri S Rajahram
Kim A Piera
Kamil Braima
Angelica F Tan
Danshy A Alaza
Bridget E Barber
Chris Drakeley
Roberto Amato
Edwin Sutanto
Hidayat Trimarsanto
Jenarun Jelip
Nicholas M Anstey
Zbynek Bozdech
Matthew Field
Matthew J Grigg
author_facet Jacob A F Westaway
Ernest Diez Benavente
Sarah Auburn
Michal Kucharski
Nicolas Aranciaga
Sourav Nayak
Timothy William
Giri S Rajahram
Kim A Piera
Kamil Braima
Angelica F Tan
Danshy A Alaza
Bridget E Barber
Chris Drakeley
Roberto Amato
Edwin Sutanto
Hidayat Trimarsanto
Jenarun Jelip
Nicholas M Anstey
Zbynek Bozdech
Matthew Field
Matthew J Grigg
author_sort Jacob A F Westaway
collection DOAJ
description Sabah, Malaysia, has amongst the highest burden of human Plasmodium knowlesi infection in the world, associated with increasing encroachment on the parasite's macaque host habitat. However, the genomic make-up of P. knowlesi in Sabah was previously poorly understood. To inform on local patterns of transmission and putative adaptive drivers, we conduct population-level genetic analyses of P. knowlesi human infections using 52 new whole genomes from Sabah, Malaysia, in combination with publicly available data. We identify the emergence of distinct geographical subpopulations within the macaque-associated clusters using identity-by-descent-based connectivity analysis. Secondly, we report on introgression events between the clusters, which may be linked to differentiation of the subpopulations, and that overlap genes critical for survival in human and mosquito hosts. Using village-level locations from P. knowlesi infections, we also identify associations between several introgressed regions and both intact forest perimeter-area ratio and mosquito vector habitat suitability. Our findings provide further evidence of the complex role of changing ecosystems and sympatric macaque hosts in Malaysia driving distinct genetic changes seen in P. knowlesi populations. Future expanded analyses of evolving P. knowlesi genetics and environmental drivers of transmission will be important to guide public health surveillance and control strategies.
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spelling doaj-art-b8a3ff0e4de044eb81ca7efb17718a542025-08-20T02:32:56ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352025-03-01193e001288510.1371/journal.pntd.0012885Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.Jacob A F WestawayErnest Diez BenaventeSarah AuburnMichal KucharskiNicolas AranciagaSourav NayakTimothy WilliamGiri S RajahramKim A PieraKamil BraimaAngelica F TanDanshy A AlazaBridget E BarberChris DrakeleyRoberto AmatoEdwin SutantoHidayat TrimarsantoJenarun JelipNicholas M AnsteyZbynek BozdechMatthew FieldMatthew J GriggSabah, Malaysia, has amongst the highest burden of human Plasmodium knowlesi infection in the world, associated with increasing encroachment on the parasite's macaque host habitat. However, the genomic make-up of P. knowlesi in Sabah was previously poorly understood. To inform on local patterns of transmission and putative adaptive drivers, we conduct population-level genetic analyses of P. knowlesi human infections using 52 new whole genomes from Sabah, Malaysia, in combination with publicly available data. We identify the emergence of distinct geographical subpopulations within the macaque-associated clusters using identity-by-descent-based connectivity analysis. Secondly, we report on introgression events between the clusters, which may be linked to differentiation of the subpopulations, and that overlap genes critical for survival in human and mosquito hosts. Using village-level locations from P. knowlesi infections, we also identify associations between several introgressed regions and both intact forest perimeter-area ratio and mosquito vector habitat suitability. Our findings provide further evidence of the complex role of changing ecosystems and sympatric macaque hosts in Malaysia driving distinct genetic changes seen in P. knowlesi populations. Future expanded analyses of evolving P. knowlesi genetics and environmental drivers of transmission will be important to guide public health surveillance and control strategies.https://doi.org/10.1371/journal.pntd.0012885
spellingShingle Jacob A F Westaway
Ernest Diez Benavente
Sarah Auburn
Michal Kucharski
Nicolas Aranciaga
Sourav Nayak
Timothy William
Giri S Rajahram
Kim A Piera
Kamil Braima
Angelica F Tan
Danshy A Alaza
Bridget E Barber
Chris Drakeley
Roberto Amato
Edwin Sutanto
Hidayat Trimarsanto
Jenarun Jelip
Nicholas M Anstey
Zbynek Bozdech
Matthew Field
Matthew J Grigg
Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.
PLoS Neglected Tropical Diseases
title Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.
title_full Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.
title_fullStr Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.
title_full_unstemmed Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.
title_short Genomic epidemiology of Plasmodium knowlesi reveals putative genetic drivers of adaptation in Malaysia.
title_sort genomic epidemiology of plasmodium knowlesi reveals putative genetic drivers of adaptation in malaysia
url https://doi.org/10.1371/journal.pntd.0012885
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