Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes

Gray, Kendall M.; Pearson, James P.; Downie, J. A.; Boboye, B.; Greenberg, E. Peter

doi:10.1128/jb.178.2.372-376.1996

Cited by 146 publications

(133 citation statements)

References 19 publications

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“…Strikingly, the luxI 1 mutant loses morphological heterogeneity and shows a faster growth rate than the wild type. This is in contrast to previous work showing growth inhibition by an autoinducer (Gray et al, 1996). Recently, it was observed that QS can induce gas vesicle formation in Serratia sp.…”

Section: Discussioncontrasting

confidence: 55%

You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae

Patzelt

Wang

Buchholz³

et al. 2013

The ISME Journal

117

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Dinoroseobacter shibae, a member of the Roseobacter clade abundant in marine environments, is characterized by a pronounced pleomorphism. Cell shapes range from variable-sized ovoid rods to long filaments with a high copy number of chromosomes. Time-lapse microscopy shows cells dividing either by binary fission or by budding from the cell poles. Here we demonstrate that this morphological heterogeneity is induced by quorum sensing (QS). D. shibae utilizes three acylated homoserine lactone (AHL) synthases (luxI 1-3 ) to produce AHLs with unsaturated C18 side chains. A DluxI 1 -knockout strain completely lacking AHL biosynthesis was uniform in morphology and divided by binary fission only. Transcriptome analysis revealed that expression of genes responsible for control of cell division was reduced in this strain, providing the link between QS and the observed phenotype. In addition, flagellar biosynthesis and type IV secretion system (T4SS) were downregulated. The wild-type phenotype and gene expression could be restored through addition of synthetic C18-AHLs. Their effectiveness was dependent on the number of double bonds in the acyl side chain and the regulated trait. The wild-type expression level of T4SS genes was fully restored even by an AHL with a saturated C18 side chain that has not been detected in D. shibae. QS induces phenotypic individualization of D. shibae cells rather than coordinating the population. This strategy might be beneficial in unpredictably changing environments, for example, during algal blooms when resource competition and grazing exert fluctuating selective pressures. A specific response towards non-native AHLs might provide D. shibae with the capacity for complex interspecies communication.

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Section: Discussioncontrasting

confidence: 55%

You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae

Patzelt

Wang

Buchholz³

et al. 2013

The ISME Journal

117

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“…The extracts were also tested with the P. aeruginosa las and rhl bioassays to determine if any of the mutant LuxI polypeptides synthesized an acylated-homoserine lactone other than N-(3-oxohexanoyl)homoserine lactone. The las bioassay can be used to detect 3-oxoacylhomoserine lactones with 8 to 14 carbons in the acyl chain (11,19), and the rhl bioassay can be used to detect butyryl or hexanoylhomoserine lactone (16,20). In addition to N-(3-oxohexanoyl)homoserine lactone, wild-type LuxI produces smaller quantities of hexanoylhomoserine lactone and N-(3-oxooctanoyl)homoserine lactone (reference 15 and unpublished data).…”

Section: Resultsmentioning

confidence: 99%

Mutational analysis of the Vibrio fischeri LuxI polypeptide: critical regions of an autoinducer synthase

et al. 1997

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Synthesis of the Vibrio fischeri autoinducer, a signal involved in the cell density-dependent activation of bioluminescence, is directed by the luxI gene product. The LuxI protein catalyzes the synthesis of N-acylhomoserine lactones from S-adenosylmethionine and acylated-acyl carrier protein. We have gained an appreciation of the LuxI regions and amino acid residues involved in autoinducer synthesis by isolating and analyzing mutations generated by random and site-specific mutagenesis of luxI. By random mutagenesis we isolated 13 different single amino acid substitutions in the LuxI polypeptide. Eleven of these substitutions resulted in no detectable autoinducer synthase activity, while the remaining two amino acid substitutions resulted in reduced but detectable activity. The substitutions that resulted in no detectable autoinducer synthase activity mapped to two small regions of LuxI. In Escherichia coli, wild-type luxI showed dominance over all of the mutations. Because autoinducer synthesis has been proposed to involve formation of a covalent bond between an acyl group and an active-site cysteine, we constructed site-directed mutations that altered each of the three cysteine residues in LuxI. All of the cysteine mutants retained substantial activity as an autoinducer synthase in E. coli. Based on the analysis of random mutations we propose a model in which there are two critical regions of LuxI, at least one of which is an intimate part of an active site, and based on the analysis of site-directed mutations we conclude that an active-site cysteine is not essential for autoinducer synthase activity.N-Acyl-homoserine lactones (commonly called autoinducers) are produced by many gram-negative bacteria and serve as intercellular signals that facilitate a phenomenon termed quorum sensing (for recent reviews see references 9, 10, 22, and 26). Quorum sensing allows a bacterial species to monitor its population density and activate specific sets of genes at a sufficiently high cell density. Regulation of luminescence in Vibrio fischeri was the first reported example of N-acyl-homoserine lactone-mediated quorum sensing, and it continues to serve as a model system (5,9,10,18,22,26). In V. fischeri, the luxR gene encodes a transcriptional regulator that activates expression of the luminescence genes in the presence of a sufficient concentration of N-(3-oxohexanoyl)homoserine lactone (7,9,10,22,26). The luxI gene encodes an autoinducer synthase that catalyzes the production of N-(3-oxohexanoyl)homoserine lactone (5, 7). There is relatively little known about the mechanism of autoinducer synthesis.Recently, LuxI from V. fischeri (24) and TraI from Agrobacterium tumefaciens (17) were shown to catalyze the synthesis of N-acyl-homoserine lactones from S-adenosylmethionine (SAM) and acylated-acyl carrier protein (ACP). These findings are consistent with proposed models for the mechanism of autoinducer synthesis (6,17,26). The models suggest that a covalent intermediate forms between an acyl group, transferred from ACP, and a ...

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“…AHL-mediated quorum sensing plays a role in regulating antibiotic biosynthesis (Wood et al, 1997), bioluminescence , plasmid conjugal transfer Piper et al, 1993), swarming , cessation of cell growth (Gray et al, 1996;Schripsema et al, 1996) and capsular polysaccharide synthesis (Beck von Bodman and Farrand, 1995). In Serratia sp.…”

mentioning

confidence: 99%

Effect of salt stress on pigment production of Serratia rubidaea N-1: A potential indicator strain for screening quorum sensing inhibitors from marine microbes

Yamazaki

Nishimura

Ishida

et al. 2006

J. Gen. Appl. Microbiol.

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Cell-to-cell signaling in the symbiotic nitrogen-fixing bacterium Rhizobium leguminosarum: autoinduction of a stationary phase and rhizosphere-expressed genes

Cited by 146 publications

References 19 publications

You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae

You are what you talk: quorum sensing induces individual morphologies and cell division modes in Dinoroseobacter shibae

Mutational analysis of the Vibrio fischeri LuxI polypeptide: critical regions of an autoinducer synthase

Effect of salt stress on pigment production of Serratia rubidaea N-1: A potential indicator strain for screening quorum sensing inhibitors from marine microbes

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