Bacterial genome adaptation to niches: Divergence of the potential virulence genes in three Burkholderia species of different survival strategies

Kim, Heenam Stanley; Schell, Mark A.; Yu, Yan; Ulrich, Ricky L.; Sarria, Saul; Nierman, William C.; DeShazer, David

doi:10.1186/1471-2164-6-174

Cited by 141 publications

(103 citation statements)

References 35 publications

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“…Burkholderia species. Burkholderia are found in a wide range of environmental niches and include host-adapted pathogens (B. mallei), opportunistic pathogens (B. pseudomallei) as well as nonpathogens such as some strains of B. thailandensis (23)(24)(25). Their genomes generally comprise two or three chromosomes of Ϸ4, 3, and 1 Mb in length, respectively.…”

Section: Resultsmentioning

confidence: 99%

Simple sequence repeats in prokaryotic genomes

Mrázek

Guo²,

Shah³

2007

Proc. Natl. Acad. Sci. U.S.A.

142

136

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Section: Resultsmentioning

confidence: 99%

Simple sequence repeats in prokaryotic genomes

Mrázek

Guo²,

Shah³

2007

Proc. Natl. Acad. Sci. U.S.A.

142

136

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“…Adaptations to avoid predation in the rhizosphere are thought to promote accidental virulence in mammals (2)(3)(4). The geographic distribution of B. pseudomallei overlaps with that of the closely related species B. thailandensis (5). Although B. thailandensis is considered relatively nonpathogenic, it has occasionally been associated with human infection, and high inocula can cause disease in mice (6)(7)(8).…”

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confidence: 99%

The Type VI Secretion System Spike Protein VgrG5 Mediates Membrane Fusion during Intercellular Spread by Pseudomallei Group Burkholderia Species

2014

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Pseudomallei group Burkholderia species are facultative intracellular parasites that spread efficiently from cell to cell by a mechanism involving the fusion of adjacent cell membranes. Intercellular fusion requires the function of the cluster 5 type VI secretion system (T6SS-5) and its associated valine-glycine repeat protein, VgrG5. Here we show that VgrG5 alleles are conserved and functionally interchangeable between Burkholderia pseudomallei and its relatives B. mallei, B. oklahomensis, and B. thailandensis. We also demonstrate that the integrity of the VgrG5 C-terminal domain is required for fusogenic activity, and we identify sequence motifs, including two hydrophobic segments, that are important for fusion. Mutagenesis and secretion experiments using B. pseudomallei strains engineered to express T6SS-5 in vitro show that the VgrG5 C-terminal domain is dispensable for T6SS-mediated secretion of Hcp5, demonstrating that the ability of VgrG5 to mediate membrane fusion can be uncoupled from its essential role in type VI secretion. We propose a model in which a unique fusogenic activity at the C terminus of VgrG5 facilitates intercellular spread by B. pseudomallei and related species following injection across the plasma membranes of infected cells.

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“…The reduced virulence of B. thailandensis is due primarily to the absence of the major capsule locus, important for B. pseudomallei virulence in mammals (4), although it is used to study the effect of type III secretion systems on phagocytic escape and retains other genes associated with virulence (5, 6). Despite virulence differences, a great deal of the core genome is shared between B. thailandensis and its relatives, including many pathways for accessory metabolism.Genes predicted to be involved in choline catabolism are found throughout the B. pseudomallei group (BPG) and Burkholderia cepacia complex (BCC) (7,8). Many soil bacteria can use choline as a sole carbon and nitrogen source, and this catabolic pathway may be particularly important for bacteria associated with eukaryotes (9).…”

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confidence: 99%

“…Genes predicted to be involved in choline catabolism are found throughout the B. pseudomallei group (BPG) and Burkholderia cepacia complex (BCC) (7,8). Many soil bacteria can use choline as a sole carbon and nitrogen source, and this catabolic pathway may be particularly important for bacteria associated with eukaryotes (9).…”

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Choline Catabolism in Burkholderia thailandensis Is Regulated by Multiple Glutamine Amidotransferase 1-Containing AraC Family Transcriptional Regulators

Nock

Wargo

2016

J Bacteriol

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Burkholderia thailandensis is a soil-dwelling bacterium that shares many metabolic pathways with the ecologically similar, but evolutionarily distant, Pseudomonas aeruginosa. Among the diverse nutrients it can utilize is choline, metabolizable to the osmoprotectant glycine betaine and subsequently catabolized as a source of carbon and nitrogen, similar to P. aeruginosa. Orthologs of genes in the choline catabolic pathway in these two bacteria showed distinct differences in gene arrangement as well as an additional orthologous transcriptional regulator in B. thailandensis. In this study, we showed that multiple glutamine amidotransferase 1 (GATase 1)-containing AraC family transcription regulators (GATRs) are involved in regulation of the B. thailandensis choline catabolic pathway (gbdR1, gbdR2, and souR). Using genetic analyses and sequencing the transcriptome in the presence and absence of choline, we identified the likely regulons of gbdR1 (BTH_II1869) and gbdR2 (BTH_II0968). We also identified a functional ortholog for P. aeruginosa souR, a GATR that regulates the metabolism of sarcosine to glycine. GbdR1 is absolutely required for expression of the choline catabolic locus, similar to P. aeruginosa GbdR, while GbdR2 is important to increase expression of the catabolic locus. Additionally, the B. thailandensis SouR ortholog (BTH_II0994) is required for catabolism of choline and its metabolites as carbon sources, whereas in P. aeruginosa, SouR function can by bypassed by GbdR. The strategy employed by B. thailandensis represents a distinct regulatory solution to control choline catabolism and thus provides both an evolutionary counterpoint and an experimental system to analyze the acquisition and regulation of this pathway during environmental growth and infection. IMPORTANCEMany proteobacteria that occupy similar environmental niches have horizontally acquired orthologous genes for metabolism of compounds useful in their shared environment. The arrangement and differential regulation of these components can help us understand both the evolution of these systems and the potential roles these pathways have in the biology of each bacterium. Here, we describe the transcriptome response of Burkholderia thailandensis to the eukaryote-enriched molecule choline, identify the regulatory pathway governing choline catabolism, and compare the pathway to that previously described for Pseudomonas aeruginosa. These data support a multitiered regulatory network in B. thailandensis, with conserved orthologs in the select agents Burkholderia pseudomallei and Burkholderia mallei, as well as the opportunistic lung pathogens in the Burkholderia cepacia clade. Burkholderia thailandensis is a saprophytic, soil-dwelling bacterium common in tropical and subtropical regions, and it is an opportunistic pathogen of insects, plants, nematodes, and amoeba (1-3). B. thailandensis is used as a less virulent model for the select agents B. pseudomallei and B. mallei, the causative agents of melioidosis and glanders, respectively. The r...

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Bacterial genome adaptation to niches: Divergence of the potential virulence genes in three Burkholderia species of different survival strategies

Cited by 141 publications

References 35 publications

Simple sequence repeats in prokaryotic genomes

Simple sequence repeats in prokaryotic genomes

The Type VI Secretion System Spike Protein VgrG5 Mediates Membrane Fusion during Intercellular Spread by Pseudomallei Group Burkholderia Species

Choline Catabolism in Burkholderia thailandensis Is Regulated by Multiple Glutamine Amidotransferase 1-Containing AraC Family Transcriptional Regulators

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