Identification of complex Plasmodium falciparum genetic backgrounds circulating in Africa: a multicountry genomic epidemiology analysis - Université de Montpellier
Article Dans Une Revue The Lancet Microbe Année : 2024

Identification of complex Plasmodium falciparum genetic backgrounds circulating in Africa: a multicountry genomic epidemiology analysis

Olivo Miotto
Alfred Amambua-Ngwa
  • Fonction : Auteur
Lucas Amenga-Etego
  • Fonction : Auteur
Muzamil Abdel Hamid
  • Fonction : Auteur
Ishag Adam
  • Fonction : Auteur
Enoch Aninagyei
Tobias Apinjoh
  • Fonction : Auteur
Gordon Awandare
  • Fonction : Auteur
Philip Bejon
  • Fonction : Auteur
Gwladys Bertin
  • Fonction : Auteur
Marielle Bouyou-Akotet
  • Fonction : Auteur
David Conway
Umberto d'Alessandro
  • Fonction : Auteur
Mahamadou Diakite
  • Fonction : Auteur
Abdoulaye Djimdé
  • Fonction : Auteur
Arjen Dondorp
Patrick Duffy
Rick Fairhurst
  • Fonction : Auteur
Caterina Fanello
  • Fonction : Auteur
Anita Ghansah
  • Fonction : Auteur
Deus Ishengoma
  • Fonction : Auteur
Mara Lawniczak
  • Fonction : Auteur
Oumou Maïga-Ascofaré
  • Fonction : Auteur
Sarah Auburn
  • Fonction : Auteur
Anna Rosanas-Urgell
  • Fonction : Auteur
Varanya Wasakul
  • Fonction : Auteur
Nina White
Alexandria Harrott
  • Fonction : Auteur
Jacob Almagro-Garcia
  • Fonction : Auteur
Richard Pearson
  • Fonction : Auteur
Sonia Goncalves
  • Fonction : Auteur
Cristina Ariani
  • Fonction : Auteur
Zbynek Bozdech
  • Fonction : Auteur
William Hamilton
  • Fonction : Auteur
Victoria Simpson
Dominic Kwiatkowski
  • Fonction : Auteur

Résumé

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.
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Dates et versions

hal-04843190 , version 1 (17-12-2024)

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Olivo Miotto, Alfred Amambua-Ngwa, Lucas Amenga-Etego, Muzamil Abdel Hamid, Ishag Adam, et al.. Identification of complex Plasmodium falciparum genetic backgrounds circulating in Africa: a multicountry genomic epidemiology analysis. The Lancet Microbe, 2024, 5 (12), pp.100941. ⟨10.1016/j.lanmic.2024.07.004⟩. ⟨hal-04843190⟩
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