Phylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa

ABSTRACT Burkholderia pseudomallei, an environmental bacterium that causes the deadly disease melioidosis, is endemic in northern Australia and Southeast Asia. An increasing number of melioidosis cases are being reported in other tropical regions, including Africa and the Indian Ocean islands. B. ps...

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Autores principales: Derek S. Sarovich, Benoit Garin, Birgit De Smet, Mirjam Kaestli, Mark Mayo, Peter Vandamme, Jan Jacobs, Palpouguini Lompo, Marc C. Tahita, Halidou Tinto, Innocente Djaomalaza, Bart J. Currie, Erin P. Price
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Publicado: American Society for Microbiology 2016
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spelling oai:doaj.org-article:a6b8c57051fe4860a61ad67be5b06fb92021-11-15T15:21:22ZPhylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa10.1128/mSphere.00089-152379-5042https://doaj.org/article/a6b8c57051fe4860a61ad67be5b06fb92016-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00089-15https://doaj.org/toc/2379-5042ABSTRACT Burkholderia pseudomallei, an environmental bacterium that causes the deadly disease melioidosis, is endemic in northern Australia and Southeast Asia. An increasing number of melioidosis cases are being reported in other tropical regions, including Africa and the Indian Ocean islands. B. pseudomallei first emerged in Australia, with subsequent rare dissemination event(s) to Southeast Asia; however, its dispersal to other regions is not yet well understood. We used large-scale comparative genomics to investigate the origins of three B. pseudomallei isolates from Madagascar and two from Burkina Faso. Phylogenomic reconstruction demonstrates that these African B. pseudomallei isolates group into a single novel clade that resides within the more ancestral Asian clade. Intriguingly, South American strains reside within the African clade, suggesting more recent dissemination from West Africa to the Americas. Anthropogenic factors likely assisted in B. pseudomallei dissemination to Africa, possibly during migration of the Austronesian peoples from Indonesian Borneo to Madagascar ~2,000 years ago, with subsequent genetic diversity driven by mutation and recombination. Our study provides new insights into global patterns of B. pseudomallei dissemination and adds to the growing body of evidence of melioidosis endemicity in Africa. Our findings have important implications for melioidosis diagnosis and management in Africa. IMPORTANCE Sporadic melioidosis cases have been reported in the African mainland and Indian Ocean islands, but until recently, these regions were not considered areas where B. pseudomallei is endemic. Given the high mortality rate of melioidosis, it is crucial that this disease be recognized and suspected in all regions of endemicity. Previous work has shown that B. pseudomallei originated in Australia, with subsequent introduction into Asia; however, the precise origin of B. pseudomallei in other tropical regions remains poorly understood. Using whole-genome sequencing, we characterized B. pseudomallei isolates from Madagascar and Burkina Faso. Next, we compared these strains to a global collection of B. pseudomallei isolates to identify their evolutionary origins. We found that African B. pseudomallei strains likely originated from Asia and were closely related to South American strains, reflecting a relatively recent shared evolutionary history. We also identified substantial genetic diversity among African strains, suggesting long-term B. pseudomallei endemicity in this region.Derek S. SarovichBenoit GarinBirgit De SmetMirjam KaestliMark MayoPeter VandammeJan JacobsPalpouguini LompoMarc C. TahitaHalidou TintoInnocente DjaomalazaBart J. CurrieErin P. PriceAmerican Society for MicrobiologyarticleBurkholderiaepidemiologyinfectious diseasemelioidosisphylogeographypopulation geneticsMicrobiologyQR1-502ENmSphere, Vol 1, Iss 2 (2016)
institution DOAJ
collection DOAJ
language EN
topic Burkholderia
epidemiology
infectious disease
melioidosis
phylogeography
population genetics
Microbiology
QR1-502
spellingShingle Burkholderia
epidemiology
infectious disease
melioidosis
phylogeography
population genetics
Microbiology
QR1-502
Derek S. Sarovich
Benoit Garin
Birgit De Smet
Mirjam Kaestli
Mark Mayo
Peter Vandamme
Jan Jacobs
Palpouguini Lompo
Marc C. Tahita
Halidou Tinto
Innocente Djaomalaza
Bart J. Currie
Erin P. Price
Phylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa
description ABSTRACT Burkholderia pseudomallei, an environmental bacterium that causes the deadly disease melioidosis, is endemic in northern Australia and Southeast Asia. An increasing number of melioidosis cases are being reported in other tropical regions, including Africa and the Indian Ocean islands. B. pseudomallei first emerged in Australia, with subsequent rare dissemination event(s) to Southeast Asia; however, its dispersal to other regions is not yet well understood. We used large-scale comparative genomics to investigate the origins of three B. pseudomallei isolates from Madagascar and two from Burkina Faso. Phylogenomic reconstruction demonstrates that these African B. pseudomallei isolates group into a single novel clade that resides within the more ancestral Asian clade. Intriguingly, South American strains reside within the African clade, suggesting more recent dissemination from West Africa to the Americas. Anthropogenic factors likely assisted in B. pseudomallei dissemination to Africa, possibly during migration of the Austronesian peoples from Indonesian Borneo to Madagascar ~2,000 years ago, with subsequent genetic diversity driven by mutation and recombination. Our study provides new insights into global patterns of B. pseudomallei dissemination and adds to the growing body of evidence of melioidosis endemicity in Africa. Our findings have important implications for melioidosis diagnosis and management in Africa. IMPORTANCE Sporadic melioidosis cases have been reported in the African mainland and Indian Ocean islands, but until recently, these regions were not considered areas where B. pseudomallei is endemic. Given the high mortality rate of melioidosis, it is crucial that this disease be recognized and suspected in all regions of endemicity. Previous work has shown that B. pseudomallei originated in Australia, with subsequent introduction into Asia; however, the precise origin of B. pseudomallei in other tropical regions remains poorly understood. Using whole-genome sequencing, we characterized B. pseudomallei isolates from Madagascar and Burkina Faso. Next, we compared these strains to a global collection of B. pseudomallei isolates to identify their evolutionary origins. We found that African B. pseudomallei strains likely originated from Asia and were closely related to South American strains, reflecting a relatively recent shared evolutionary history. We also identified substantial genetic diversity among African strains, suggesting long-term B. pseudomallei endemicity in this region.
format article
author Derek S. Sarovich
Benoit Garin
Birgit De Smet
Mirjam Kaestli
Mark Mayo
Peter Vandamme
Jan Jacobs
Palpouguini Lompo
Marc C. Tahita
Halidou Tinto
Innocente Djaomalaza
Bart J. Currie
Erin P. Price
author_facet Derek S. Sarovich
Benoit Garin
Birgit De Smet
Mirjam Kaestli
Mark Mayo
Peter Vandamme
Jan Jacobs
Palpouguini Lompo
Marc C. Tahita
Halidou Tinto
Innocente Djaomalaza
Bart J. Currie
Erin P. Price
author_sort Derek S. Sarovich
title Phylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa
title_short Phylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa
title_full Phylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa
title_fullStr Phylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa
title_full_unstemmed Phylogenomic Analysis Reveals an Asian Origin for African <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> and Further Supports Melioidosis Endemicity in Africa
title_sort phylogenomic analysis reveals an asian origin for african <named-content content-type="genus-species">burkholderia pseudomallei</named-content> and further supports melioidosis endemicity in africa
publisher American Society for Microbiology
publishDate 2016
url https://doaj.org/article/a6b8c57051fe4860a61ad67be5b06fb9
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