Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model

Chandler, Josephine R.; Heilmann, Silja; Mittler, John E.; Greenberg, E. Peter

doi:10.1038/ismej.2012.69

Cited by 87 publications

(131 citation statements)

References 49 publications

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“…MalR might be a degenerate AHL quorum-sensing signal receptor. There is increasing evidence that AHL receptors play an important role in interspecies competition (30,31). Antibiotics and cytotoxic factors are often activated by AHL quorum sensing (31)(32)(33), and as discussed above, MalR (11) and QscR (29) are antibiotic activated.…”

Section: Discussionmentioning

confidence: 99%

A Burkholderia thailandensis Acyl-Homoserine Lactone-Independent Orphan LuxR Homolog That Activates Production of the Cytotoxin Malleilactone

et al. 2015

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Burkholderia thailandensis has three acyl-homoserine lactone (AHL) LuxR-LuxI quorum-sensing circuits and two orphan LuxR homologs. Orphans are LuxR-type transcription factors that do not have cognate LuxI-type AHL synthases. One of the orphans, MalR, is genetically linked to the mal gene cluster, which encodes enzymes required for production of the cytotoxic polyketide malleilactone. Under normal laboratory conditions the mal gene cluster is silent; however, antibiotics like trimethoprim induce mal transcription. We show that trimethoprim-dependent induction of the mal genes requires MalR. MalR has all of the conserved amino acid residues characteristic of AHL-responsive LuxR homologs, but in B. thailandensis, MalR activation of malleilactone synthesis genes is not responsive to AHLs. MalR can activate transcription from the mal promoter in E. coli without addition of AHLs or trimethoprim. Expression of malR in B. thailandensis is induced by trimethoprim. Our data indicate that MalR binds to a lux box-like element in the mal promoter and activates transcription of the mal genes in an AHL-independent manner. Antibiotics like trimethoprim appear to activate mal gene expression indirectly by somehow activating malR expression. MalR activation of the mal genes represents an example of a LuxR homolog that is not a receptor for an AHL quorum-sensing signal. Our evidence is consistent with the idea that mal gene activation depends solely on sufficient transcription of the malR gene. A cyl-homoserine lactone (AHL) quorum-sensing systems are widespread among the Proteobacteria. AHLs are generated by members of the LuxI family of AHL synthases. Members of the LuxR protein family serve as cognate AHL-dependent transcription factors. Often, the genes targeted by LuxR family members have an 18-to 20-base inverted repeat in their promoter regions that shows conservation across species. These repeat elements are called lux box-like sequences and serve as binding sites for the transcription factors. Sequence identity in pairwise comparisons of LuxR polypeptides is rather limited (18 to 35%), but there is a conserved N-terminal AHL binding region and a conserved C-terminal DNA binding region where sequence identity is higher and where there are highly conserved residues (see references 1 and 2 for reviews).Burkholderia thailandensis has three pairs of luxI-luxR-type genes called btaI1-btaR1, btaI2-btaR2, and btaI3-btaR3. Each of the luxR homologs is linked to its cognate luxI homolog, as is the case for luxI-luxR-type gene pairs in many other bacteria. This species also has two additional luxR homologs, btaR4 (now called malR [see below]) and btaR5 (3). LuxR family members like MalR and BtaR5 are called orphans (4) or solos (5), because the genes encoding these polypeptides are not associated with a luxI homolog. Relatively few orphans have been characterized. Some orphans, like Pseudomonas aeruginosa QscR or Salmonella enterica serovar Typhimurium SdiA, show complete conservation of all of the invariant residues in the ...

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Section: Discussionmentioning

confidence: 99%

A Burkholderia thailandensis Acyl-Homoserine Lactone-Independent Orphan LuxR Homolog That Activates Production of the Cytotoxin Malleilactone

et al. 2015

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“…Chandler et al demonstrated this fact recently in a coculture model using the soil saprophytes Burkholderia thailandensis and Chromobacterium violaceum (145). Bruns et al demonstrated that signaling compounds were able to trigger microbial growth (146).…”

Section: Signaling Compoundsmentioning

confidence: 98%

The Rebirth of Culture in Microbiology through the Example of Culturomics To Study Human Gut Microbiota

et al. 2015

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SUMMARY Bacterial culture was the first method used to describe the human microbiota, but this method is considered outdated by many researchers. Metagenomics studies have since been applied to clinical microbiology; however, a “dark matter” of prokaryotes, which corresponds to a hole in our knowledge and includes minority bacterial populations, is not elucidated by these studies. By replicating the natural environment, environmental microbiologists were the first to reduce the “great plate count anomaly,” which corresponds to the difference between microscopic and culture counts. The revolution in bacterial identification also allowed rapid progress. 16S rRNA bacterial identification allowed the accurate identification of new species. Mass spectrometry allowed the high-throughput identification of rare species and the detection of new species. By using these methods and by increasing the number of culture conditions, culturomics allowed the extension of the known human gut repertoire to levels equivalent to those of pyrosequencing. Finally, taxonogenomics strategies became an emerging method for describing new species, associating the genome sequence of the bacteria systematically. We provide a comprehensive review on these topics, demonstrating that both empirical and hypothesis-driven approaches will enable a rapid increase in the identification of the human prokaryote repertoire.

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“…These extracellular products are often important for nutrient acquisition, interspecies competition, or virulence (6)(7)(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).…”

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.

110

169

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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...

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Acyl-homoserine lactone-dependent eavesdropping promotes competition in a laboratory co-culture model

Cited by 87 publications

References 49 publications

A Burkholderia thailandensis Acyl-Homoserine Lactone-Independent Orphan LuxR Homolog That Activates Production of the Cytotoxin Malleilactone

A Burkholderia thailandensis Acyl-Homoserine Lactone-Independent Orphan LuxR Homolog That Activates Production of the Cytotoxin Malleilactone

The Rebirth of Culture in Microbiology through the Example of Culturomics To Study Human Gut Microbiota

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

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