AI-3 synthesis is not dependent on luxS in Escherichia coli

Matthew Walters, Marcelo P. Sircili, Vanessa Sperandio

Research output: Contribution to journalArticle

127 Citations (Scopus)

Abstract

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 5-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.

Original languageEnglish (US)
Pages (from-to)5668-5681
Number of pages14
JournalJournal of Bacteriology
Volume188
Issue number16
DOIs
StatePublished - Aug 2006

Fingerprint

Homocysteine
Quorum Sensing
Escherichia coli
Mutation
Phenotype
Adenosylhomocysteinase
S-Adenosylhomocysteine
Enterohemorrhagic Escherichia coli
Amino Acid Transport Systems
Oxaloacetic Acid
Aromatic Amino Acids
Aspartic Acid
Pseudomonas aeruginosa
Virulence
Tyrosine
Glutamic Acid
N-octanoylhomoserine lactone
Bacteria
Enzymes
Genes

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Immunology

Cite this

AI-3 synthesis is not dependent on luxS in Escherichia coli. / Walters, Matthew; Sircili, Marcelo P.; Sperandio, Vanessa.

In: Journal of Bacteriology, Vol. 188, No. 16, 08.2006, p. 5668-5681.

Research output: Contribution to journalArticle

Walters, Matthew ; Sircili, Marcelo P. ; Sperandio, Vanessa. / AI-3 synthesis is not dependent on luxS in Escherichia coli. In: Journal of Bacteriology. 2006 ; Vol. 188, No. 16. pp. 5668-5681.
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