Burkholderia pseudomallei distribution in Australasia is linked to paleogeographic and anthropogenic history

Baker, Anthony L.; Pearson, Talima; Sahl, Jason W.; Hepp, Crystal M.; Price, Erin P.; Sarovich, Derek S.; Mayo, Mark; Tuanyok, Apichai; Currie, Bart J.; Keim, Paul; Warner, Jeffrey

doi:10.1371/journal.pone.0206845

Cited by 13 publications

(19 citation statements)

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“…1 A). A similar theory has been postulated for B. pseudomallei populations in Papua New Guinea, the Sahul land bridge between Australia and New Guinea during the last ice age 43 . It is also worthy of note, however that genetic analysis of humans from Myanmar and Southwestern China (~ 6,000 individuals) demonstrated that these individuals share haplogroups (sharing a common ancestor) 44 , with individuals from China migrating to Burma likely along river valleys that connect Myanmar and China (e.g.…”

Section: Discussionsupporting

confidence: 68%

Myanmar Burkholderia pseudomallei strains are genetically diverse and originate from Asia with phylogenetic evidence of reintroductions from neighbouring countries

Webb

Win

Zin

et al. 2020

Sci Rep

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Melioidosis was first identified in Myanmar in 1911 but for the last century it has remained largely unreported there. Burkholderia pseudomallei was first isolated from the environment of Myanmar in 2016, confirming continuing endemicity. Recent genomic studies showed that B. pseudomallei originated in Australia and spread to Asia, with phylogenetic evidence of repeated reintroduction of B. pseudomallei across countries bordered by the Mekong River and the Malay Peninsula. We present the first whole-genome sequences of B. pseudomallei isolates from Myanmar: nine clinical and seven environmental isolates. We used large-scale comparative genomics to assess the genetic diversity, phylogeography and potential origins of B. pseudomallei in Myanmar. Global phylogenetics demonstrated that Myanmar isolates group in two distantly related clades that reside in a more ancestral Asian clade with high amounts of genetic diversity. The diversity of B. pseudomallei from Myanmar and divergence within our global phylogeny suggest that the original introduction of B. pseudomallei to Myanmar was not a recent event. Our study provides new insights into global patterns of B. pseudomallei dissemination, most notably the dynamic nature of movement of B. pseudomallei within densely populated Southeast Asia. The role of anthropogenic influences in both ancient and more recent dissemination of B. pseudomallei to Myanmar and elsewhere in Southeast Asia and globally requires further study.

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Section: Discussionsupporting

confidence: 68%

Myanmar Burkholderia pseudomallei strains are genetically diverse and originate from Asia with phylogenetic evidence of reintroductions from neighbouring countries

Webb

Win

Zin

et al. 2020

Sci Rep

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“…pseudomallei populations, the Wallace line, has limited the dissemination of B. pseudomallei , encouraged its divergent evolution, and ensured the paucity of genotypic or phylogenetic overlap between the two known hyperendemicity foci [72, 73]. However, in the phylogeny presented in this study, five B.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies [12,17,21] have used WGS analyses to identify single introduction event of B. pseudomallei from Australia to Asia. The oceanic biogeographic barrier between Asian and Australasian B. pseudomallei populations, the Wallace line, has limited the dissemination of B. pseudomallei, encouraged its divergent evolution, and ensured the paucity of genotypic or phylogenetic overlap between the two known hyperendemicity foci [72,73]. However, in the phylogeny presented in this study, five B. pseudomallei strains (SAMN04208629, SAMN04208630, SAMN04208605, SAMN04208593, and SAMN02443741) from Thailand clustered into two distinct clades inside the Australian group (group 5), suggesting a close genetic background and several historical transmission events from Australia to Thailand.…”

Section: Discussionmentioning

confidence: 99%

Genetic diversity and transmission patterns of Burkholderia pseudomallei on Hainan island, China, revealed by a population genomics analysis

et al. 2021

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Burkholderia pseudomallei is a Gram-negative soil-dwelling bacillus that causes melioidosis, a frequently fatal infectious disease, in tropical and subtropical regions. Previous studies have identified the overall genetic and evolutionary characteristics of B. pseudomallei on a global scale, including its origin and transmission routes. However, beyond its known hyperendemicity foci in northern Australia and Southeast Asia, the distribution and genetic characteristics of B. pseudomallei in most tropical regions remain poorly understood, including in southern China. Here, we sequenced the genomes of 122 B. pseudomallei strains collected from Hainan, an island in southern China, in 2002–2018, to investigate the population structure, relationships with global strains, local epidemiology, and virulence and antimicrobial-resistance factors. A phylogenetic analysis and hierarchical clustering divided the Hainan strains into nine phylogenic groups (PGs), 80 % of which were concentrated within five major groups (group 1: corresponding to minor sequence types [STs], 12.3 %; group 3: ST46 and ST50, 31.1 %; group 9: ST58, 13.1 %; group 11: ST55, 8.2 %; group 15: mainly ST658, 15.6%). A phylogenetic analysis that included global strains suggested that B. pseudomallei in Hainan originated from Southeast Asian countries, transmitted in multiple historical importation events. We also identified several mutual transmission events between Hainan and Southeast Asian countries in recent years, including three importation events from Thailand and Singapore to Hainan and three exportation events from Hainan to Singapore, Malaysia, and Taiwan island. A statistical analysis of the temporal distribution showed that the Hainan strains of groups 3, 9, and 15 have dominated the disease epidemic locally in the last 5 years. The spatial distribution of the Hainan strains demonstrated that some PGs are distributed in different cities on Hainan island, and by combining phylogenic and geographic distribution information, we detected 21 between-city transmission events, indicating its frequent local transmission. The detection of virulence factor genes showed that 56 % of the Hainan strains in group 1 encode a B. pseudomallei -specific adherence factor, boaB, confirming the specific pathogenic characteristics of the Hainan strains in group 1. An analysis of the antimicrobial-resistance potential of B. pseudomallei showed that various kinds of alterations were identified in clinically relevant antibiotic resistance factors, such as AmrR, PenA and PBP3, etc. Our results clarify the population structure, local epidemiology, and pathogenic characteristics of B. pseudomallei in Hainan, providing further insight into its regional and global transmission networks and improving our knowledge of its global phylogeography.

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“…Bootstrap values were of very high confidence across both trees at the ST-261 and ST-259 clades despite branch collapse and phylogenetic incongruence in the mixed dataset. Of further concern, the phylogeny containing MSHR163_Mixed caused incorrect geographic assignment of the Papua New Guinean clade, unexpectedly shifting its known grouping with Australian strains [9, 49] to the Asian clade; this incorrect placement received very high bootstrap support (Figure 5B). Reconstructing the global phylogeny sans MSHR1631_Mixed resolved both issues (Figure 5A).…”

Section: Resultsmentioning

confidence: 99%

Comparative genomics confirms a rare melioidosis human-to-human transmission event and reveals incorrect phylogenomic reconstruction due to polyclonality

Aziz

Currie

Mayo

et al. 2019

Preprint

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21Human-to-human transmission of the melioidosis bacterium, Burkholderia pseudomallei, is exceedingly 22 rare, with only a handful of suspected cases documented to date. Here, we used whole-genome sequencing 23 (WGS) to characterise one such unusual B. pseudomallei transmission event, which occurred between a 24 breastfeeding mother with mastitis and her child. Two strains corresponding to multilocus sequence types 25 (STs) 259 and 261 were identified in the mother's sputum from both the primary culture sweep and in 26 purified colonies, confirming an unusual polyclonal infection in this patient. In contrast, primary culture 27 sweeps of the mother's breast milk and the child's cerebrospinal fluid and blood samples contained only 28 ST-259, indicating monoclonal transmission to the child. Analysis of purified ST-259 isolates showed no 29 genetic variation between mother and baby isolates, providing the strongest possible evidence of B. 30 pseudomallei transmission, probably via breastfeeding. Next, phylogenomic analysis of all isolates, 31 including the mother's mixed ST-259/261 sputum sample was performed to investigate the effects of 32 mixtures on phylogenetic inference. Inclusion of this mixture caused a dramatic reduction in the number 33 of informative SNPs, resulting in branch collapse of ST-259 and ST-261 isolates, and several instances of 34 incorrect topology in a global B. pseudomallei phylogeny, resulting in phylogenetic incongruence. Although 35 phylogenomics can provide clues about the presence of mixtures within WGS datasets, our results 36demonstrate that this methodology can lead to phylogenetic misinterpretation if mixed genomes are not 37 correctly identified and omitted. Using current bioinformatic tools, we demonstrate a robust method for 38 bacterial mixture identification and strain parsing that avoids these pitfalls. 393 Impact Statement 40Burkholderia pseudomallei is the causative agent of melioidosis, a tropical disease of high mortality. B. 41 pseudomallei infections occur almost exclusively through contact with contaminated soil and water. Using 42 whole-genome sequencing (WGS), we investigated a rare case of suspected B. pseudomallei transmission 43 from mother to child. The mother's sputum, breast milk and the baby's blood and cerebrospinal fluid (CSF) 44 specimens were collected, and DNA was extracted from both pure colonies and primary culture sweeps to 45 capture potential strain mixtures. In-depth analysis of genetic variants identified two strains in the mother's 46 sputum belonging to multilocus sequence types ST-259 and ST-261, whereas the child was infected with 47 only ST-259. Comparative genomics revealed no genetic differences between mother and child ST-259 48 isolates, providing the strongest possible evidence of transmission to the child via breast milk. The sputum 49 strain mixture was subsequently used to develop a bioinformatic method for identification and 50 quantification of mixtures from WGS data. Using this method, we found ST-259 and ST-261 at an 87%:13% 51 rat...

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Burkholderia pseudomallei distribution in Australasia is linked to paleogeographic and anthropogenic history

Cited by 13 publications

References 44 publications

Myanmar Burkholderia pseudomallei strains are genetically diverse and originate from Asia with phylogenetic evidence of reintroductions from neighbouring countries

Myanmar Burkholderia pseudomallei strains are genetically diverse and originate from Asia with phylogenetic evidence of reintroductions from neighbouring countries

Genetic diversity and transmission patterns of Burkholderia pseudomallei on Hainan island, China, revealed by a population genomics analysis

Comparative genomics confirms a rare melioidosis human-to-human transmission event and reveals incorrect phylogenomic reconstruction due to polyclonality

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