Role of quorum sensing in the pathogenicity of Burkholderia pseudomallei

Ulrich, Ricky L.; DeShazer, David; Brueggemann, Ernst E.; Hines, Harry B.; Oyston, Petra C. F.; Jeddeloh, Jeffrey A.

doi:10.1099/jmm.0.45661-0

Cited by 104 publications

(105 citation statements)

References 46 publications

Supporting

Mentioning

102

Contrasting

Order By: Relevance

“…In B. glumae, TofI-R regulates toxoflavin production, motility, protein secretion, and QsmR, an isocitrate lyase regulatortype transcriptional regulator (10)(11)(12). Less is known about gene control by C8-HSL in B. thailandensis via BtaI-R and B. pseudomallei via BpsI-R (13)(14)(15). In the present study, we found that QS induces cellular enzymes for production of oxalate (HOOC-COOH), which is excreted into the culture medium and likely shared by other members of the population, and as such is a public good.…”

mentioning

confidence: 99%

Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress

Goo

Majerczyk

et al. 2012

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

112

169

View full text Add to dashboard Cite

Acyl-homoserine lactone-mediated quorum sensing (QS) regulates diverse activities in many species of Proteobacteria. QS-controlled genes commonly code for production of secreted or excreted public goods. The acyl-homoserine lactones are synthesized by members of the LuxI signal synthase family and are detected by cognate members of the LuxR family of transcriptional regulators. QS affords a means of population density-dependent gene regulation. Control of public goods via QS provides a fitness benefit. Another potential role for QS is to anticipate overcrowding. As population density increases and stationary phase approaches, QS might induce functions important for existence in stationary phase. Here we provide evidence that in three related species of the genus Burkholderia QS allows individuals to anticipate and survive stationary-phase stress. Survival requires QS-dependent activation of cellular enzymes required for production of excreted oxalate, which serves to counteract ammonia-mediated alkaline toxicity during stationary phase. Our findings provide an example of QS serving as a means to anticipate stationary phase or life at the carrying capacity of a population by activating the expression of cytoplasmic enzymes, altering cellular metabolism, and producing a shared resource or public good, oxalate.Burkholderia carrying capacity | glumae | pseudomallei | thailandensis | cell death A cyl-homoserine lactone (AHL)-mediated quorum sensing (QS) regulates diverse activities, including bioluminescence, biofilm formation, motility, and virulence factor formation, in many Proteobacteria (1-3). AHLs are synthesized most typically by members of the LuxI family signal synthases and detected by members of the LuxR family of transcriptional regulators (1-3). A large body of work has characterized the molecular mechanisms of bacterial QS; demonstrating the population-wide benefits that drive QS-mediated cooperative behavior has proven difficult, however. Cooperative activities benefit individuals within a group (4, 5).QS-controlled genes commonly code for the production of extracellular public goods that can be shared by all members of the group regardless of which members produce them. These extracellular products are often important for nutrient acquisition, interspecies competition, or virulence (6-8). In Pseudomonas aeruginosa, QS control of secreted proteases provides fitness benefits, because the proteases are produced only when they can be used efficiently (9). Other potential roles of QS in bacteria have been proposed, including the hypothesis that QS enables bacteria to anticipate population carrying capacity in a given environment. Anticipation of stationary phase might allow individuals to modify their physiology in preparation for survival at population carrying capacity.Here we address the question of whether QS is involved in anticipation of stationary-phase stress in three closely related bacteria: the rice pathogen Burkholderia glumae, the opportunistic human pathogen Burkholderia pseudomallei, and the...

show abstract

mentioning

confidence: 99%

Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress

Goo

Majerczyk

et al. 2012

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

112

169

View full text Add to dashboard Cite

show abstract

“…1). Our genome analysis in silico indicated that the B. pseudomallei and B. mallei QS networks are genetically similar, and as with B. pseudomallei, B. mallei does not encode a putative LuxS system ( (34,35). It has been proposed that microbial species carrying multiple luxIR genes obtain these alleles through horizontal gene transfer (16).…”

Section: Discussionmentioning

confidence: 99%

“…For human and plant pathogens, AHL-based communication systems allow a microbial community to strategically induce or repress expression of genes, specifically alleles encoding putative virulence factors, in response to environmental stimuli. Several reports have identified functional QS systems in various Burkholderia species and have shown that these bacterial communication networks both positively and negatively regulate numerous extracellular virulence factors in addition to contributing to animal pathogenicity (B. cepacia) (1,3,20,21,31,34,36).…”

Section: Discussionmentioning

confidence: 99%

“…Functional QS networks have recently been identified in Burkholderia cepacia, Burkholderia vietnamiensis, Burkholderia thailandensis, and Burkholderia pseudomallei (1,3,15,20,32,(34)(35)(36). Collectively, these Burkholderia QS networks have been shown to both positively and negatively regulate various cellular processes, including AHL and protease production, siderophore biosynthesis, biofilm formation, lipase and betahemolytic activities, swarming and twitching motilities, and substrate utilization (18,20,21,32,35,36).…”

mentioning

confidence: 99%

“…Collectively, these Burkholderia QS networks have been shown to both positively and negatively regulate various cellular processes, including AHL and protease production, siderophore biosynthesis, biofilm formation, lipase and betahemolytic activities, swarming and twitching motilities, and substrate utilization (18,20,21,32,35,36). Furthermore, disruption of these cell signaling systems has been shown to reduce the pathogenicity of B. cepacia and Burkholderia pseudomallei in murine and hamster models of infection (1,31,34,36).…”

mentioning

confidence: 99%

See 2 more Smart Citations

Quorum Sensing: a Transcriptional Regulatory System Involved in the Pathogenicity of Burkholderia mallei

Ulrich¹,

DeShazer²,

Hines

et al. 2004

Infect Immun

Self Cite

View full text Add to dashboard Cite

Numerous gram-negative bacterial pathogens regulate virulence factor expression by using a cell density mechanism termed quorum sensing (QS). An in silico analysis of the Burkholderia mallei ATCC 23344 genome revealed that it encodes at least two luxI and four luxR homologues. Using mass spectrometry, we showed that wild-type B. mallei produces the signaling molecules N-octanoyl-homoserine lactone and N-decanoyl-homoserine lactone. To determine if QS is involved in the virulence of B. mallei, we generated mutations in each putative luxIR homologue and tested the pathogenicities of the derivative strains in aerosol BALB/c mouse and intraperitoneal hamster models. Disruption of the B. mallei QS alleles, especially in RJ16 (bmaII) and RJ17 (bmaI3), which are luxI mutants, significantly reduced virulence, as indicated by the survival of mice who were aerosolized with 10 4 CFU (10 50% lethal doses [LD 50 s]). For the B. mallei transcriptional regulator mutants (luxR homologues), mutation of the bmaR5 allele resulted in the most pronounced decrease in virulence, with 100% of the challenged animals surviving a dose of 10 LD 50 s. Using a Syrian hamster intraperitoneal model of infection, we determined the LD 50 s for wild-type B. mallei and each QS mutant. An increase in the relative LD 50 was found for RJ16 (bmaI1) (>967 CFU), RJ17 (bmaI3) (115 CFU), and RJ20 (bmaR5) (151 CFU) compared to wild-type B. mallei (<13 CFU). These findings demonstrate that B. mallei carries multiple luxIR homologues that either directly or indirectly regulate the biosynthesis of an essential virulence factor(s) that contributes to the pathogenicity of B. mallei in vivo.

show abstract

Production of the Quorum‐Sensing Molecules N‐Acylhomoserine Lactones by Endobacteria Associated with Mortierella alpina A‐178

et al. 2012

View full text Add to dashboard Cite

Gram‐negative bacteria communicate with one another using N‐acylhomoserine lactones (AHLs) as signaling molecules. This mechanism, known as quorum sensing (QS), is needed to develop pathogenicity, as well as symbiotic interactions with eukaryotic hosts, such as animals and plants. Increasing evidence indicates that certain bacteria, namely endobacteria, also inhabit fungal cells and establish symbiotic relationships with their hosts. However, it has not been clear whether bacterial QS acts in developing the relationships. Here we describe the isolation and identification of N‐heptanoylhomoserine lactone and N‐octanoylhomoserine lactone from the culture broth of the zygomycete fungus Mortierella alpina A‐178. This suggested the presence of endobacteria in the fungus, as was confirmed by PCR, fluorescence in situ hybridization, and transmission electron microscopy. Two major bands obtained by PCR‐denaturing gradient gel electrophoresis showed sequence identity to genes in the β‐proteobacterium Castellaniella defragrans (100 %) and the Gram‐positive bacterium Cryobacterium sp. (99.8 %). The production of AHLs depended on the presence of endobacteria and was induced in response to the increase in the concentration of AHLs, suggesting that the bacterium conducts AHL‐mediated QS in the fungus. This paper is the first to report the production of AHLs by endofungal bacteria and raises the possibility that QS plays roles in the development of fungus–endobacterium symbiosis.

show abstract

Role of quorum sensing in the pathogenicity of Burkholderia pseudomallei

Cited by 104 publications

References 46 publications

Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress

Bacterial quorum sensing, cooperativity, and anticipation of stationary-phase stress

Quorum Sensing: a Transcriptional Regulatory System Involved in the Pathogenicity of Burkholderia mallei

Production of the Quorum‐Sensing Molecules N‐Acylhomoserine Lactones by Endobacteria Associated with Mortierella alpina A‐178

Contact Info

Product

Resources

About