Identification of complex Plasmodium falciparum genetic backgrounds circulating in Africa: a multicountry genomic epidemiology analysis
Issued Date
2024-01-01
Resource Type
eISSN
26665247
Scopus ID
2-s2.0-85208670211
Journal Title
The Lancet Microbe
Rights Holder(s)
SCOPUS
Bibliographic Citation
The Lancet Microbe (2024)
Suggested Citation
Miotto O., Amambua-Ngwa A., Amenga-Etego L.N., Abdel Hamid M.M., Adam I., Aninagyei E., Apinjoh T., Awandare G.A., Bejon P., Bertin G.I., Bouyou-Akotet M., Claessens A., Conway D.J., D'Alessandro U., Diakite M., Djimdé A., Dondorp A.M., Duffy P., Fairhurst R.M., Fanello C.I., Ghansah A., Ishengoma D.S., Lawniczak M., Maïga-Ascofaré O., Auburn S., Rosanas-Urgell A., Wasakul V., White N.F.D., Harrott A., Almagro-Garcia J., Pearson R.D., Goncalves S., Ariani C., Bozdech Z., Hamilton W.L., Simpson V., Kwiatkowski D.P. Identification of complex Plasmodium falciparum genetic backgrounds circulating in Africa: a multicountry genomic epidemiology analysis. The Lancet Microbe (2024). doi:10.1016/j.lanmic.2024.07.004 Retrieved from: https://repository.li.mahidol.ac.th/handle/20.500.14594/102058
Title
Identification of complex Plasmodium falciparum genetic backgrounds circulating in Africa: a multicountry genomic epidemiology analysis
Author(s)
Miotto O.
Amambua-Ngwa A.
Amenga-Etego L.N.
Abdel Hamid M.M.
Adam I.
Aninagyei E.
Apinjoh T.
Awandare G.A.
Bejon P.
Bertin G.I.
Bouyou-Akotet M.
Claessens A.
Conway D.J.
D'Alessandro U.
Diakite M.
Djimdé A.
Dondorp A.M.
Duffy P.
Fairhurst R.M.
Fanello C.I.
Ghansah A.
Ishengoma D.S.
Lawniczak M.
Maïga-Ascofaré O.
Auburn S.
Rosanas-Urgell A.
Wasakul V.
White N.F.D.
Harrott A.
Almagro-Garcia J.
Pearson R.D.
Goncalves S.
Ariani C.
Bozdech Z.
Hamilton W.L.
Simpson V.
Kwiatkowski D.P.
Amambua-Ngwa A.
Amenga-Etego L.N.
Abdel Hamid M.M.
Adam I.
Aninagyei E.
Apinjoh T.
Awandare G.A.
Bejon P.
Bertin G.I.
Bouyou-Akotet M.
Claessens A.
Conway D.J.
D'Alessandro U.
Diakite M.
Djimdé A.
Dondorp A.M.
Duffy P.
Fairhurst R.M.
Fanello C.I.
Ghansah A.
Ishengoma D.S.
Lawniczak M.
Maïga-Ascofaré O.
Auburn S.
Rosanas-Urgell A.
Wasakul V.
White N.F.D.
Harrott A.
Almagro-Garcia J.
Pearson R.D.
Goncalves S.
Ariani C.
Bozdech Z.
Hamilton W.L.
Simpson V.
Kwiatkowski D.P.
Author's Affiliation
Université des Sciences, des Techniques et des Technologies de Bamako
Kampala International University in Tanzania
Mahidol Oxford Tropical Medicine Research Unit
University of Health and Allied Sciences, Ghana
Laboratory of Pathogen Host Interactions
School of Biological Sciences
Université des Sciences de la Santé Libreville
Noguchi Memorial Institute for Medical Research
Institute of Endemic Diseases Sudan
National Institute for Medical Research Tanga
University of Buea
Wellcome Trust Research Laboratories Nairobi
London School of Hygiene & Tropical Medicine
IRD Institut de Recherche pour le Developpement
Prins Leopold Instituut voor Tropische Geneeskunde
Menzies School of Health Research
Qassim University
Bernhard Nocht Institut fur Tropenmedizin Hamburg
University of Ghana
National Institute of Allergy and Infectious Diseases (NIAID)
Nuffield Department of Medicine
Wellcome Sanger Institute
Kampala International University in Tanzania
Mahidol Oxford Tropical Medicine Research Unit
University of Health and Allied Sciences, Ghana
Laboratory of Pathogen Host Interactions
School of Biological Sciences
Université des Sciences de la Santé Libreville
Noguchi Memorial Institute for Medical Research
Institute of Endemic Diseases Sudan
National Institute for Medical Research Tanga
University of Buea
Wellcome Trust Research Laboratories Nairobi
London School of Hygiene & Tropical Medicine
IRD Institut de Recherche pour le Developpement
Prins Leopold Instituut voor Tropische Geneeskunde
Menzies School of Health Research
Qassim University
Bernhard Nocht Institut fur Tropenmedizin Hamburg
University of Ghana
National Institute of Allergy and Infectious Diseases (NIAID)
Nuffield Department of Medicine
Wellcome Sanger Institute
Corresponding Author(s)
Other Contributor(s)
Abstract
Background: The population structure of the malaria parasite Plasmodium falciparum can reveal underlying adaptive evolutionary processes. Selective pressures to maintain complex genetic backgrounds can encourage inbreeding, producing distinct parasite clusters identifiable by population structure analyses. Methods: We analysed population structure in 3783 P falciparum genomes from 21 countries across Africa, provided by the MalariaGEN Pf7 dataset. We used Principal Coordinate Analysis to cluster parasites, identity by descent (IBD) methods to identify genomic regions shared by cluster members, and linkage analyses to establish their co-inheritance patterns. Structural variants were reconstructed by de novo assembly and verified by long-read sequencing. Findings: We identified a strongly differentiated cluster of parasites, named AF1, comprising 47 (1·2%) of 3783 samples analysed, distributed over 13 countries across Africa, at locations over 7000 km apart. Members of this cluster share a complex genetic background, consisting of up to 23 loci harbouring many highly differentiated variants, rarely observed outside the cluster. IBD analyses revealed common ancestry at these loci, irrespective of sampling location. Outside the shared loci, however, AF1 members appear to outbreed with sympatric parasites. The AF1 differentiated variants comprise structural variations, including a gene conversion involving the dblmsp and dblmsp2 genes, and numerous single nucleotide polymorphisms. Several of the genes harbouring these mutations are functionally related, often involved in interactions with red blood cells including invasion, egress, and erythrocyte antigen export. Interpretation: We propose that AF1 parasites have adapted to some unidentified evolutionary niche, probably involving interactions with host erythrocytes. This adaptation involves a complex compendium of interacting variants that are rarely observed in Africa, which remains mostly intact despite recombination events. The term cryptotype was used to describe a common background interspersed with genomic regions of local origin. Funding: Bill & Melinda Gates Foundation.