Phylogenomic Analysis Reveals an Asian Origin for African Burkholderia pseudomallei and Further Supports Melioidosis Endemicity in Africa.
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.
Global and Tropical Health Division, Menzies School of Health Research, Darwin, Australia.
Derek S
0000-0002-6944-3980
DS
Sarovich
Bacteriological Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.
Benoit
B
Garin
Department of Clinical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Faculty of Sciences, Laboratory of Microbiology, Ghent University, Ghent, Belgium.
Birgit
B
De Smet
Global and Tropical Health Division, Menzies School of Health Research, Darwin, Australia.
Mirjam
M
Kaestli
Global and Tropical Health Division, Menzies School of Health Research, Darwin, Australia.
Mark
M
Mayo
Faculty of Sciences, Laboratory of Microbiology, Ghent University, Ghent, Belgium.
Peter
P
Vandamme
Department of Clinical Sciences, Institute of Tropical Medicine, Antwerp, Belgium; Department of Microbiology and Immunology, University of Leuven, Leuven, Belgium.
Jan
J
Jacobs
Clinical Research Unit of Nanoro (IRSS-CRUN), Nanoro, Burkina Faso.
Palpouguini
P
Lompo
Clinical Research Unit of Nanoro (IRSS-CRUN), Nanoro, Burkina Faso.
Marc C
MC
Tahita
Clinical Research Unit of Nanoro (IRSS-CRUN), Nanoro, Burkina Faso.
Halidou
H
Tinto
Androva University Hospital, Mahajanga, Madagascar.
Innocente
I
Djaomalaza
Global and Tropical Health Division, Menzies School of Health Research, Darwin, Australia.
Bart J
BJ
Currie
Global and Tropical Health Division, Menzies School of Health Research, Darwin, Australia.
Erin P
0000-0002-1079-4882
EP
Price
Burkholderia; epidemiology; infectious disease; melioidosis; phylogeography; population genetics