The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolates
Abstract Background The frequent communication between African and Southeast Asian (SEA) countries has led to the risk of imported malaria cases in the China-Myanmar border (CMB) region. Therefore, tracing the origins of new malaria infections is important in the maintenance of malaria-free zones in...
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BMC
2024-12-01
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| Series: | Parasites & Vectors |
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| Online Access: | https://doi.org/10.1186/s13071-024-06629-3 |
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| author | Yini Tian Run Ye Dongmei Zhang Yilong Zhang |
| author_facet | Yini Tian Run Ye Dongmei Zhang Yilong Zhang |
| author_sort | Yini Tian |
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| description | Abstract Background The frequent communication between African and Southeast Asian (SEA) countries has led to the risk of imported malaria cases in the China-Myanmar border (CMB) region. Therefore, tracing the origins of new malaria infections is important in the maintenance of malaria-free zones in this border region. A new genotyping tool based on a robust mitochondrial (mt) /apicoplast (apico) barcode was developed to estimate genetic diversity and infer the evolutionary history of Plasmodium falciparum across the major distribution ranges. However, the mt/apico genomes of P. falciparum isolates from the CMB region to date are poorly characterized, even though this region is highly endemic to P. falciparum malaria. Methods We have sequenced the whole mt/apico genome of 34 CMB field isolates and utilized a published data set of 147 mt/apico genome sequences to present global genetic diversity and to revisit the evolutionary history of the CMB P. falciparum. Results Genetic differentiation based on mt/apico genome of P. falciparum revealed that the CMB (Lazan, Myanmar) isolates presented high genetic diversity with several characteristics of ancestral populations and shared many of the genetic features with West Thailand (Mae Sot; WTH) and to some extent West African (Banjul, Gambia; Navrongo, Ghana; WAF) isolates. The reconstructed haplotype network displayed that the CMB and WTH P. falciparum isolates have the highest representation (five) in the five ancestral (central) haplotypes (H1, H2, H4, H7, and H8), which are comparatively older than isolates from other SEA populations as well as the WAF populations. In addition, the highest estimate of the time to the Most Recent Common Ancestor (TMRCA) of 42,400 (95% CI 18,300–82100) years ago was presented by the CMB P. falciparum compared to the other regional populations. The statistically significant negative values of Fu's Fs with unimodal distribution in pairwise mismatch distribution curves indicate past demographic expansions in CMB P. falciparum with slow population expansion between approximately 12,500–20,000 ybp. Conclusions The results on the complete mt/apico genome sequence analysis of the CMB P. falciparum indicated high genetic diversity with ancient population expansion and TMRCA, and it seems probable that P. falciparum might have existed in CMB, WTH, and WAF for a long time before being introduced into other Southeast Asian countries or regions. To reduce the impact of sample size or geographic bias on the estimate of the evolutionary timeline, future studies need to expand the range of sample collection and ensure the representativeness of samples across geographic distributions. Additionally, by mapping global patterns of mt/apico genome polymorphism, we will gain valuable insights into the evolutionary history of P. falciparum and optimised strategies for controlling P. falciparum malaria at international borders. Graphical Abstract |
| format | Article |
| id | doaj-art-cf6db1b83b614dbe98a69cf7a58a8c7e |
| institution | Kabale University |
| issn | 1756-3305 |
| language | English |
| publishDate | 2024-12-01 |
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| spelling | doaj-art-cf6db1b83b614dbe98a69cf7a58a8c7e2025-01-05T12:10:04ZengBMCParasites & Vectors1756-33052024-12-0117111110.1186/s13071-024-06629-3The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolatesYini Tian0Run Ye1Dongmei Zhang2Yilong Zhang3Department of Tropical Diseases, Faculty of Naval Medicine, Naval Medical UniversityDepartment of Tropical Diseases, Faculty of Naval Medicine, Naval Medical UniversityDepartment of Tropical Diseases, Faculty of Naval Medicine, Naval Medical UniversityDepartment of Tropical Diseases, Faculty of Naval Medicine, Naval Medical UniversityAbstract Background The frequent communication between African and Southeast Asian (SEA) countries has led to the risk of imported malaria cases in the China-Myanmar border (CMB) region. Therefore, tracing the origins of new malaria infections is important in the maintenance of malaria-free zones in this border region. A new genotyping tool based on a robust mitochondrial (mt) /apicoplast (apico) barcode was developed to estimate genetic diversity and infer the evolutionary history of Plasmodium falciparum across the major distribution ranges. However, the mt/apico genomes of P. falciparum isolates from the CMB region to date are poorly characterized, even though this region is highly endemic to P. falciparum malaria. Methods We have sequenced the whole mt/apico genome of 34 CMB field isolates and utilized a published data set of 147 mt/apico genome sequences to present global genetic diversity and to revisit the evolutionary history of the CMB P. falciparum. Results Genetic differentiation based on mt/apico genome of P. falciparum revealed that the CMB (Lazan, Myanmar) isolates presented high genetic diversity with several characteristics of ancestral populations and shared many of the genetic features with West Thailand (Mae Sot; WTH) and to some extent West African (Banjul, Gambia; Navrongo, Ghana; WAF) isolates. The reconstructed haplotype network displayed that the CMB and WTH P. falciparum isolates have the highest representation (five) in the five ancestral (central) haplotypes (H1, H2, H4, H7, and H8), which are comparatively older than isolates from other SEA populations as well as the WAF populations. In addition, the highest estimate of the time to the Most Recent Common Ancestor (TMRCA) of 42,400 (95% CI 18,300–82100) years ago was presented by the CMB P. falciparum compared to the other regional populations. The statistically significant negative values of Fu's Fs with unimodal distribution in pairwise mismatch distribution curves indicate past demographic expansions in CMB P. falciparum with slow population expansion between approximately 12,500–20,000 ybp. Conclusions The results on the complete mt/apico genome sequence analysis of the CMB P. falciparum indicated high genetic diversity with ancient population expansion and TMRCA, and it seems probable that P. falciparum might have existed in CMB, WTH, and WAF for a long time before being introduced into other Southeast Asian countries or regions. To reduce the impact of sample size or geographic bias on the estimate of the evolutionary timeline, future studies need to expand the range of sample collection and ensure the representativeness of samples across geographic distributions. Additionally, by mapping global patterns of mt/apico genome polymorphism, we will gain valuable insights into the evolutionary history of P. falciparum and optimised strategies for controlling P. falciparum malaria at international borders. Graphical Abstracthttps://doi.org/10.1186/s13071-024-06629-3Evolutionary historyChina-Myanmar borderMitochondrialApicoplastPlasmodium falciparum |
| spellingShingle | Yini Tian Run Ye Dongmei Zhang Yilong Zhang The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolates Parasites & Vectors Evolutionary history China-Myanmar border Mitochondrial Apicoplast Plasmodium falciparum |
| title | The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolates |
| title_full | The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolates |
| title_fullStr | The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolates |
| title_full_unstemmed | The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolates |
| title_short | The evolutionary history of Plasmodium falciparum from mitochondrial and apicoplast genomes of China-Myanmar border isolates |
| title_sort | evolutionary history of plasmodium falciparum from mitochondrial and apicoplast genomes of china myanmar border isolates |
| topic | Evolutionary history China-Myanmar border Mitochondrial Apicoplast Plasmodium falciparum |
| url | https://doi.org/10.1186/s13071-024-06629-3 |
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