Suspected cases of intracontinental Burkholderia pseudomallei sequence type homoplasy resolved using whole-genome sequencing

Aziz, Ammar; Sarovich, Derek S.; Harris, Tegan M.; Kaestli, Mirjam; McRobb, Evan; Mayo, Mark; Currie, Bart J.; Price, Erin P.

doi:10.1099/mgen.0.000139

Cited by 26 publications

(29 citation statements)

References 34 publications

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“…Based on comparative analysis of 175 genomes, isolates with the same ST but mixed LPS type did not group together (Fig 4: “ST homoplasy cases”) and were separated by a large number of SNPs. This is comparable to previously observed MLST homoplasy in B. pseudomallei (20, 21). To assess the effect of recombination on phylogenetic inference, SNP density filtering was applied to remove recombinogenic SNPs with Gubbins (v.2.3.1), which did not considerably alter the topology of the phylogenetic tree (data not shown).…”

Section: Resultssupporting

confidence: 91%

Tracing the environmental footprint of theBurkholderia pseudomalleilipopolysaccharide genotypes in the tropical “Top End” of the Northern Territory, Australia

Webb

Rachlin

Rigas

et al. 2019

Preprint

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The Tier 1 select agentBurkholderia pseudomalleiis an environmental bacterium that causes melioidosis, a high mortality disease. Variably present genetic markers used to elucidate strain origin, relatedness and virulence inB. pseudomalleiinclude theBurkholderiaintracellular motility factor A (bimA) and filamentous hemagglutinin 3 (fhaB3) gene variants. Three lipopolysaccharide (LPS) O-antigen types inB. pseudomalleihave been described, which vary in proportion between Australian and Asian isolates. However, it remains unknown if these LPS types can be used as genetic markers for geospatial analysis within a contiguous melioidosis-endemic region. Using a combination of whole-genome sequencing (WGS), statistical analysis and geographical mapping, we examined if the LPS types can be used as geographical markers in the Northern Territory, Australia. The clinical isolates revealed that LPS A prevalence was highest in the Darwin and surrounds (n = 660; 96% being LPS A and 4% LPS B) and LPS B in the Katherine and Katherine remote and East Arnhem regions (n = 79; 60% being LPS A and 40% LPS B). Bivariate logistics regression of 999 clinicalB. pseudomalleiisolates revealed that the odds of getting a clinical isolate with LPS B was highest in East Arnhem in comparison to Darwin and surrounds (OR 19.5, 95% CI 9.1 – 42.0;p<0.001). This geospatial correlation was subsequently confirmed by geographically mapping the LPS type from 340 environmental Top End strains. We also found that in the Top End, the minoritybimAgenotypebimABmhas a similar remote region geographical footprint to that of LPS B. In addition, correlation of LPS type with multi-locus sequence typing (MLST) was strong, and where multiple LPS types were identified within a single sequence type, WGS confirmed homoplasy of the MLST loci. The clinical, sero-diagnostic and vaccine implications of geographically-basedB. pseudomalleiLPS types, and their relationships to regional and global dispersal of melioidosis, require global collaborations with further analysis of larger clinically and geospatially-linked datasets.Author SummaryBurkholderia pseudomalleiis a pathogenic soil bacterium that causes the disease melioidosis, which occurs in many tropical regions globally and in recent years has emerged in non-tropical regions. Melioidosis has been predicted to affect 165,000 people every year resulting in an estimated 89,000 deaths. Person to person transmission is rare with most cases linked to exposure to the bacterium from the environment. The genetic background ofB. pseudomalleihas been well studied and variably present genes have been linked to distinct melioidosis disease states and geographic regions, however we still need a stronger understanding of the association of genes with geography. Three lipopolysaccharide types exist inB. pseudomalleiand the prevalence of the lipopolysaccharide genes vary between melioidosis endemic regions, but it is unknown if the lipopolysaccharide genes can be used as geographical markers in a single melioidosis-endemic region. In this study, we used a combination of whole-genome sequencing, statistics and geographical mapping to elucidate if the three lipopolysaccharide genes can be used as geographical markers within the Northern Territory, Australia. We show that the three LPS types have distinct but overlapping geographical footprints within a single melioidosis region and can be used as geographic markers alongside a number of other important variably presentB. pseudomalleigenes.

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Section: Resultssupporting

confidence: 91%

Tracing the environmental footprint of theBurkholderia pseudomalleilipopolysaccharide genotypes in the tropical “Top End” of the Northern Territory, Australia

Webb

Rachlin

Rigas

et al. 2019

Preprint

Self Cite

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“…Populations of B. pseudomallei are ecologically established and individual strain types are typically found less than 50 linear kilometres from one another in the environment 6,7,17 . Despite this, distinct genetic populations of the bacterium have only been documented across larger geographical boundaries, including the robust partitioning of Asian and Australian isolates at Wallace's Line 7,12,13,38 . To-date, the smallest physical separation of B. pseudomallei populations identified has been amongst isolates from the Northern Territory, Australia and north Queensland, Australia 9 .…”

Section: Discussionmentioning

confidence: 99%

Whole-genome sequencing of Burkholderia pseudomallei from an urban melioidosis hot spot reveals a fine-scale population structure and localised spatial clustering in the environment

Rachlin

Mayo

Webb

et al. 2020

Sci Rep

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Melioidosis is a severe disease caused by the environmental bacterium Burkholderia pseudomallei that affects both humans and animals throughout northern Australia, Southeast Asia and increasingly globally. While there is a considerable degree of genetic diversity amongst isolates, B. pseudomallei has a robust global biogeographic structure and genetic populations are spatially clustered in the environment. We examined the distribution and local spread of B. pseudomallei in Darwin, northern territory, Australia, which has the highest recorded urban incidence of melioidosis globally. We sampled soil and land runoff throughout the city centre and performed whole-genome sequencing (WGS) on B. pseudomallei isolates. By combining phylogenetic analyses, Bayesian clustering and spatial hot spot analysis our results demonstrate that some sequence types (STs) are widespread in the urban Darwin environment, while others are highly spatially clustered over a small geographic scale. this clustering matches the spatial distribution of clinical cases for one St. Results also demonstrate a greater overall isolate diversity recovered from drains compared to park soils, further supporting the role drains may play in dispersal of B. pseudomallei Sts in the environment. collectively, knowledge gained from this study will allow for better understanding of B. pseudomallei phylogeography and melioidosis source attribution, particularly on a local level. Burkholderia pseudomallei is an environmental Gram-negative bacillus and the causative agent of melioidosis, a potentially fatal infection of humans and animals 1. Regions of high B. pseudomallei endemicity predominantly include Southeast Asia and northern Australia, though the bacterium is also increasingly found in other tropical regions including the Indian subcontinent, Africa and the Americas 2. Melioidosis is typically considered noncommunicable with direct person-to-person transmission and zoonotic disease being remarkably rare 3,4. Nearly all B. pseudomallei infections are caused by a single direct exposure event to contaminated soil or surface water in the environment and individual cases of melioidosis are typically the result of infection by different strains of the bacterium 5. A limited geographic dispersal of B. pseudomallei strains has also been identified and the bacterium is now recognised as being ecologically established and spatially clustered in the environment 6-8. This is in spite of the frequent opportunities B. pseudomallei has to spread within the water table, via agricultural and migratory animals, or in transported soil 6,9-11. This restricted geographical distribution has resulted in distinct genetic populations of the bacterium, which are evident despite high levels of gene recombination and sequence type (ST)

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“…Changes in the world′s climate is likely to have an effect on the range and transmission of B. pseudomallei ; a rise in the sea surface and ambient temperature may lead to an increase in melioidosis cases in Australia [ 40 ]. The genetic diversity of B. pseudomallei populations has been characterised by using multilocus sequence typing (MLST); however, due to its high recombination rate, B. pseudomallei isolates may share the same MLST despite being genetically and geographically distinct [ 93 ]. Therefore, whole-genome sequencing—which may not always be readily available—is required to identify strain origin in cases where the same ST is identified between geographically-different locations.…”

Section: Current and Future Challengesmentioning

confidence: 99%

Melioidosis: An Australian Perspective

2018

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Burkholderia pseudomallei is endemic in northern Australia, with cases of melioidosis most commonly occurring during the wet season in individuals with diabetes, hazardous alcohol use, and chronic kidney disease. Pneumonia is the most common presentation and the majority of patients are bacteraemic—however, infection may involve almost any organ, with the skin and soft tissues, genitourinary system, visceral organs, and bone and joints affected most commonly. Central nervous system involvement is rarer, but has a high attributable mortality. Increased awareness of the disease amongst healthcare providers, ready access to appropriate antibiotic therapy and high-quality intensive care services has resulted in a sharp decline in the case fatality rate over the last 20 years. Further improvement in clinical outcomes will require a greater understanding of the disease′s pathophysiology, its optimal management, and more effective strategies for its prevention.

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Suspected cases of intracontinental Burkholderia pseudomallei sequence type homoplasy resolved using whole-genome sequencing

Cited by 26 publications

References 34 publications

Tracing the environmental footprint of theBurkholderia pseudomalleilipopolysaccharide genotypes in the tropical “Top End” of the Northern Territory, Australia

Tracing the environmental footprint of theBurkholderia pseudomalleilipopolysaccharide genotypes in the tropical “Top End” of the Northern Territory, Australia

Whole-genome sequencing of Burkholderia pseudomallei from an urban melioidosis hot spot reveals a fine-scale population structure and localised spatial clustering in the environment

Melioidosis: An Australian Perspective

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