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Journal of Bacteriology, August 2006, p. 5668-5681, Vol. 188, No. 16
0021-9193/06/$08.00+0     doi:10.1128/JB.00648-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

AI-3 Synthesis Is Not Dependent on luxS in Escherichia coli{dagger}

Matthew Walters,1 Marcelo P. Sircili,2 and Vanessa Sperandio1*

Department of Microbiology, University of Texas Southwestern Medical Center, Dallas, Texas 75390-9048,1 Instituto Butantan, Sao Paulo, Brazil 05503-9002

Received 5 May 2006/ Accepted 2 June 2006

The quorum-sensing (QS) signal autoinducer-2 (AI-2) has been proposed to promote interspecies signaling in a broad range of bacterial species. AI-2 is spontaneously derived from 4,5-dihydroxy-2,3-pentanedione that, along with homocysteine, is produced by cleavage of S-adenosylhomocysteine (SAH) and S-ribosylhomocysteine by the Pfs and LuxS enzymes. Numerous phenotypes have been attributed to AI-2 QS signaling using luxS mutants. We have previously reported that the luxS mutation also affects the synthesis of the AI-3 autoinducer that activates enterohemorrhagic Escherichia coli virulence genes. Here we show that several species of bacteria synthesize AI-3, suggesting a possible role in interspecies bacterial communication. The luxS mutation leaves the cell with only one pathway, involving oxaloacetate and L-glutamate, for de novo synthesis of homocysteine. The exclusive use of this pathway for homocysteine production appears to alter metabolism in the luxS mutant, leading to decreased levels of AI-3. The addition of aspartate and expression of an aromatic amino acid transporter, as well as a tyrosine-specific transporter, restored AI-3-dependent phenotypes in an luxS mutant. The defect in AI-3 production, but not in AI-2 production, in the luxS mutant was restored by expressing the Pseudomonas aeruginosa S-adenosylhomocysteine hydrolase that synthesizes homocysteine directly from SAH. Furthermore, phenotype microarrays revealed that the luxS mutation caused numerous metabolic deficiencies, while AI-3 signaling had little effect on metabolism. This study examines how AI-3 production is affected by the luxS mutation and explores the roles of the LuxS/AI-2 system in metabolism and QS.

* Corresponding author. Mailing address: University of Texas Southwestern Medical Center, Department of Microbiology, 5323 Harry Hines Blvd., Dallas, TX 75390-9048. Phone: (214) 648-1603. Fax: (214) 648-5905. E-mail: Vanessa.Sperandio{at}UTSouthwestern.edu.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, August 2006, p. 5668-5681, Vol. 188, No. 16
0021-9193/06/$08.00+0     doi:10.1128/JB.00648-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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