Genomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in Ethiopia
Abstract Ethiopia has the greatest burden of Plasmodium vivax in Africa, but little is known about the epidemiological landscape of parasites across the country. We analysed the genomic diversity of 137 P. vivax isolates collected nine Ethiopian districts from 2012 to 2016. Signatures of selection w...
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| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-11-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-023-47889-w |
| _version_ | 1797415469028737024 |
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| author | Alebachew Messele Kebede Edwin Sutanto Hidayat Trimarsanto Ernest Diez Benavente Mariana Barnes Richard D. Pearson Sasha V. Siegel Berhanu Erko Ashenafi Assefa Sisay Getachew Abraham Aseffa Beyene Petros Eugenia Lo Rezika Mohammed Daniel Yilma Angela Rumaseb Francois Nosten Rintis Noviyanti Julian C. Rayner Dominic P. Kwiatkowski Ric N. Price Lemu Golassa Sarah Auburn |
| author_facet | Alebachew Messele Kebede Edwin Sutanto Hidayat Trimarsanto Ernest Diez Benavente Mariana Barnes Richard D. Pearson Sasha V. Siegel Berhanu Erko Ashenafi Assefa Sisay Getachew Abraham Aseffa Beyene Petros Eugenia Lo Rezika Mohammed Daniel Yilma Angela Rumaseb Francois Nosten Rintis Noviyanti Julian C. Rayner Dominic P. Kwiatkowski Ric N. Price Lemu Golassa Sarah Auburn |
| author_sort | Alebachew Messele Kebede |
| collection | DOAJ |
| description | Abstract Ethiopia has the greatest burden of Plasmodium vivax in Africa, but little is known about the epidemiological landscape of parasites across the country. We analysed the genomic diversity of 137 P. vivax isolates collected nine Ethiopian districts from 2012 to 2016. Signatures of selection were detected by cross-country comparisons with isolates from Thailand (n = 104) and Indonesia (n = 111), representing regions with low and high chloroquine resistance respectively. 26% (35/137) of Ethiopian infections were polyclonal, and 48.5% (17/35) of these comprised highly related clones (within-host identity-by-descent > 25%), indicating frequent co-transmission and superinfection. Parasite gene flow between districts could not be explained entirely by geographic distance, with economic and cultural factors hypothesised to have an impact on connectivity. Amplification of the duffy binding protein gene (pvdbp1) was prevalent across all districts (16–75%). Cross-population haplotype homozygosity revealed positive selection in a region proximal to the putative chloroquine resistance transporter gene (pvcrt-o). An S25P variant in amino acid transporter 1 (pvaat1), whose homologue has recently been implicated in P. falciparum chloroquine resistance evolution, was prevalent in Ethiopia (96%) but not Thailand or Indonesia (35–53%). The genomic architecture in Ethiopia highlights circulating variants of potential public health concern in an endemic setting with evidence of stable transmission. |
| first_indexed | 2024-03-09T05:49:03Z |
| format | Article |
| id | doaj.art-5386a2335ef64870878c33d75df801c1 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-09T05:49:03Z |
| publishDate | 2023-11-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-5386a2335ef64870878c33d75df801c12023-12-03T12:18:57ZengNature PortfolioScientific Reports2045-23222023-11-0113111610.1038/s41598-023-47889-wGenomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in EthiopiaAlebachew Messele Kebede0Edwin Sutanto1Hidayat Trimarsanto2Ernest Diez Benavente3Mariana Barnes4Richard D. Pearson5Sasha V. Siegel6Berhanu Erko7Ashenafi Assefa8Sisay Getachew9Abraham Aseffa10Beyene Petros11Eugenia Lo12Rezika Mohammed13Daniel Yilma14Angela Rumaseb15Francois Nosten16Rintis Noviyanti17Julian C. Rayner18Dominic P. Kwiatkowski19Ric N. Price20Lemu Golassa21Sarah Auburn22Aklilu Lemma Institute of Pathobiology, Addis Ababa UniversityExeins Health InitiativeMenzies School of Health Research and Charles Darwin UniversityLaboratory of Experimental Cardiology, Department of Cardiology, University Medical Center UtrechtMenzies School of Health Research and Charles Darwin UniversityWellcome Sanger InstituteWellcome Sanger InstituteAklilu Lemma Institute of Pathobiology, Addis Ababa UniversityEthiopian Public Health InstituteArmauer Hansen Research Unit (AHRI)Armauer Hansen Research Unit (AHRI)Addis Ababa UniversityDepartment of Microbiology and Immunology, College of Medicine, Drexel UniversityUniversity of GondarJimma University Clinical Trial Unit, Department of Internal Medicine, Jimma UniversityMenzies School of Health Research and Charles Darwin UniversityShoklo Malaria Research Unit, Faculty of Tropical Medicine, Mahidol UniversityEijkman Institute for Molecular BiologyCambridge Institute for Medical Research, University of CambridgeWellcome Sanger InstituteMenzies School of Health Research and Charles Darwin UniversityAklilu Lemma Institute of Pathobiology, Addis Ababa UniversityMenzies School of Health Research and Charles Darwin UniversityAbstract Ethiopia has the greatest burden of Plasmodium vivax in Africa, but little is known about the epidemiological landscape of parasites across the country. We analysed the genomic diversity of 137 P. vivax isolates collected nine Ethiopian districts from 2012 to 2016. Signatures of selection were detected by cross-country comparisons with isolates from Thailand (n = 104) and Indonesia (n = 111), representing regions with low and high chloroquine resistance respectively. 26% (35/137) of Ethiopian infections were polyclonal, and 48.5% (17/35) of these comprised highly related clones (within-host identity-by-descent > 25%), indicating frequent co-transmission and superinfection. Parasite gene flow between districts could not be explained entirely by geographic distance, with economic and cultural factors hypothesised to have an impact on connectivity. Amplification of the duffy binding protein gene (pvdbp1) was prevalent across all districts (16–75%). Cross-population haplotype homozygosity revealed positive selection in a region proximal to the putative chloroquine resistance transporter gene (pvcrt-o). An S25P variant in amino acid transporter 1 (pvaat1), whose homologue has recently been implicated in P. falciparum chloroquine resistance evolution, was prevalent in Ethiopia (96%) but not Thailand or Indonesia (35–53%). The genomic architecture in Ethiopia highlights circulating variants of potential public health concern in an endemic setting with evidence of stable transmission.https://doi.org/10.1038/s41598-023-47889-w |
| spellingShingle | Alebachew Messele Kebede Edwin Sutanto Hidayat Trimarsanto Ernest Diez Benavente Mariana Barnes Richard D. Pearson Sasha V. Siegel Berhanu Erko Ashenafi Assefa Sisay Getachew Abraham Aseffa Beyene Petros Eugenia Lo Rezika Mohammed Daniel Yilma Angela Rumaseb Francois Nosten Rintis Noviyanti Julian C. Rayner Dominic P. Kwiatkowski Ric N. Price Lemu Golassa Sarah Auburn Genomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in Ethiopia Scientific Reports |
| title | Genomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in Ethiopia |
| title_full | Genomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in Ethiopia |
| title_fullStr | Genomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in Ethiopia |
| title_full_unstemmed | Genomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in Ethiopia |
| title_short | Genomic analysis of Plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in Ethiopia |
| title_sort | genomic analysis of plasmodium vivax describes patterns of connectivity and putative drivers of adaptation in ethiopia |
| url | https://doi.org/10.1038/s41598-023-47889-w |
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