Phylogeographic, genomic, and meropenem susceptibility analysis of Burkholderia ubonensis

Price, Erin P.; Sarovich, Derek S.; Webb, Jessica R.; Hall, Carina M.; Jaramillo, Sierra A; Sahl, Jason W.; Kaestli, Mirjam; Mayo, Mark; Harrington, Glenda; Baker, Anthony L.; Sidak-Loftis, Lindsay C; Settles, Erik W.; Lummis, Madeline; Schupp, James M.; Gillece, John D.; Tuanyok, Apichai; Warner, Jeffrey; Busch, Joseph D.; Keim, Paul; Currie, Bart J.; Wagner, David M.

doi:10.1371/journal.pntd.0005928

Cited by 19 publications

(14 citation statements)

References 74 publications

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“…Orthologous core biallelic single-nucleotide polymorphisms (SNPs) and insertion and deletion events (InDels) were identified from WGS data using Genome Analysis Toolkit (GATK) in SPANDx v3.2 50 . The closed Australian B. pseudomallei genome MSHR1153 51 was used as the reference for read mapping (N50:4,032,226 bp, contigs:2, total length:7,312,903 bp) and trees were rooted with MSHR0668, the most ancestral B. pseudomallei isolate identified to date based on a previous study 52 . A maximum-parsimony (MP) tree was constructed from 134,032 core orthologous SNPs and Indels using PAUP (v4.0a165) 53 with 100 bootstrap replicates.…”

Section: Genome Assembly and Phylogenetic Reconstructionmentioning

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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Section: Genome Assembly and Phylogenetic Reconstructionmentioning

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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“…High-level MEM r has not yet been reported in B. pseudomallei, but decreased susceptibility to MEM occurring over the course of melioidosis therapy has been documented (16). However, the recent discovery that highly MEM r strains of B. ubonensis, a nonpathogenic Bcc member, are frequently coisolated from the environment with B. pseudomallei raised the specter of potential horizontal resistance gene transfer between the two species (21).…”

Section: Discussionmentioning

confidence: 99%

“…Burkholderia ubonensis strain Bu278, also known as Bp8955, is a soil isolate from Juncos, Puerto Rico, that is MEM r (MIC, Ն32 g/ml) (21). Strain MSMB2152 is a soil isolate from the Northern Territory, Australia, and MEM susceptible (MIC, 2 to 3 g/ml) (21). Mutants derived from these strains are listed in Table S1 in the supplemental material.…”

Section: Methodsmentioning

confidence: 99%

“…PenB from a highly carbapenem-resistant B. ubonensis strain confers increased resistance to a susceptible B. ubonensis strain. Although MEM r in B. ubonensis is not uncommon, strains from diverse geographical sources, including the Northern Territory of Australia and Puerto Rico, exhibit a wide range of susceptibilities (MICs, 2 g/ml to Ն32 g/ml) (21,35). To assess whether PenB from the highly carbapenem-resistant strain Bu278 was sufficient to bestow resistance on the carbapenem-susceptible B. ubonensis strain MSMB2152, we examined the relative contributions of PenB from strains Bu278 (PenB Bu278 ) and MSMB2152 (PenB MSMB2152 ) to MEM and IMP resistance in the Bu278 and MSMB2152 ΔpenB derivatives Bu312 and Bu410, respectively (Table 6).…”

Section: Identification Of B Ubonensis Mutants With Reduced Meropenementioning

confidence: 99%

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Burkholderia ubonensis Meropenem Resistance: Insights into Distinct Properties of Class A β-Lactamases in Burkholderia cepacia Complex and Burkholderia pseudomallei Complex Bacteria

Somprasong

Hall

Webb

et al. 2020

mBio

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Burkholderia pseudomallei, the founding member of the B. pseudomallei complex (Bpc), is a biothreat agent and causes melioidosis, a disease whose treatment mainly relies on ceftazidime and meropenem. The concern is that B. pseudomallei could enhance its drug resistance repertoire by the acquisition of DNA from resistant near-neighbor species. Burkholderia ubonensis, a member of the B. cepacia complex (Bcc), is commonly coisolated from environments where B. pseudomallei is present. Unlike B. pseudomallei, in which significant primary carbapenem resistance is rare, it is not uncommon in B. ubonensis, but the underlying mechanisms are unknown. We established that carbapenem resistance in B. ubonensis is due to an inducible class A PenB β-lactamase, as has been shown for other Bcc bacteria. Inducibility is not sufficient for high-level resistance but also requires other determinants, such as a PenB that is more robust than that present in susceptible isolates, as well as other resistance factors. Curiously and diagnostic for the two complexes, both Bpc and Bcc bacteria contain distinct annotated PenA class A β-lactamases. However, the protein from Bcc bacteria is missing its essential active-site serine and, therefore, is not a β-lactamase. Regulated expression of a transcriptional penB′-lacZ (β-galactosidase) fusion in the B. pseudomallei surrogate B. thailandensis confirms that although Bpc bacteria lack an inducible β-lactamase, they contain the components required for responding to aberrant peptidoglycan synthesis resulting from β-lactam challenge. Understanding the diversity of antimicrobial resistance in Burkholderia species is informative about how the challenges arising from potential resistance transfer between them can be met. IMPORTANCE Burkholderia pseudomallei causes melioidosis, a tropical disease that is highly fatal if not properly treated. Our data show that, in contrast to B. pseudomallei, B. ubonensis β-lactam resistance is fundamentally different because intrinsic resistance is mediated by an inducible class A β-lactamase. This includes resistance to carbapenems. Our work demonstrates that studies with near-neighbor species are informative about the diversity of antimicrobial resistance in Burkholderia and can also provide clues about the potential of resistance transfer between bacteria inhabiting the same environment. Knowledge about potential adverse challenges resulting from the horizontal transfer of resistance genes between members of the two complexes enables the design of effective countermeasures.

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“…In bald eagles, the most common species belonging to this phylum were tentatively classified as Burkholderia ubonensis and Delftia tsuruhatensis , comprising 18% and 10% of all fecal bacteria detected respectively. Both are common environmental bacteria that have been occasionally linked to infections in humans [38, 39]. B. ubonensis was also detected in the two common ravens sampled, ranking seventh most common and averaging 5.6%.…”

Section: Discussionmentioning

confidence: 99%

Bacterial Diversity in Feces of Wild Bald Eagles, Turkey Vultures and Common Ravens from the Pacific Northwest Coast, U.S.A

Crespo

Dowd²,

Varland³

et al. 2019

Preprint

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RC) 28 29 30 ¶ These authors contributed equally to this work. 2 31 Abstract 32Birds harbor diverse microorganisms in their guts, which collectively fulfill important 33 roles in providing their hosts with nutrition and protection from pathogens. Although numerous 34 studies have investigated the presence of certain pathogenic bacteria in the feces of wild birds, 35 only a few have attempted to investigate the microbiota of the gut. This study analyzed the avian 36 bacteria present in the cloaca of avian scavengers captured on coastal beaches of Washington and 37 Oregon between 2013 and 2015: 10 turkey vultures (Cathartes aura), 9 bald eagles (Haliaeetus 38 leucocephalus), and 2 common ravens (Corvus corax). We used illumina sequencing based on 39 the V4 region of the 16s gene was to characterize the bacterial diversity. Our investigation 40 revealed phylum-level differences in the microbiome of turkey vultures, compared with bald 41 eagles and common ravens. Substantial microbiome differences were found between bald eagles 42 and ravens below the phylum level. Although little is known about the possible relations among 43 these microorganisms, our analyses provides the first integrated look at the composition of the 44 avian microbiota and serves as a foundation for future studies in this area. 45 46 Keywords: avian scavenger, turkey vulture, bald eagle, common raven, bacteria, coast, 47 microbiota, microbiome, raptor. 48 Abbreviations: OTU = operational taxonomic unit 49 50 3 51 Introduction 52 Birds harbor diverse microorganisms in their gut, which collectively fulfill important 53 roles in providing their hosts with nutrition and protection from pathogens [1]. Gut 54 microorganisms have been isolated and characterized by a variety of methods, such as culture-55 based assays, culture-independent DNA sequencing, and fluorescence in situ hybridization 56 targeting the 16S rRNA gene [2]. Most of these studies are limited in scope and are focused on 57 pathogenic bacteria such as Salmonella, Escherichia coli, Campylobacter, and Clostridium 58 perfringens [3-5]. 59 In recent years, metagenomics using next-generation sequencing has emerged as a way to 60 analyze complex microbial communities and their functions [6]. This approach is capable of 61 sequencing thousands or millions of amplified DNA molecules in a single run and, for bacteria, 62 does not require conventional cloning and amplification. Additionally, metagenomic studies 63 offer a powerful tool for the comprehensive and unbiased assessment of microbial diversity 64 within the complex gut ecosystem by allowing examination of organisms not easily cultured in 65 the laboratory [6, 7]. 66 Few studies have used genetic sequencing to explore the intestinal microbiota of wild 67 birds [8]. Furthermore, these studies reported gene sequences to phylum or class levels only, 68 with no attempt to understand extant microorganism populations at the species level. In this 69 study, we analyze the avian microbiome present in the cloaca of bald eagles, turkey vultures, ...

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Phylogeographic, genomic, and meropenem susceptibility analysis of Burkholderia ubonensis

Cited by 19 publications

References 74 publications

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

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

Burkholderia ubonensis Meropenem Resistance: Insights into Distinct Properties of Class A β-Lactamases in Burkholderia cepacia Complex and Burkholderia pseudomallei Complex Bacteria

Bacterial Diversity in Feces of Wild Bald Eagles, Turkey Vultures and Common Ravens from the Pacific Northwest Coast, U.S.A

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