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Research Paper |
Institute of Infections and Immunity, University of Nottingham, Queen’s Medical Centre, Nottingham NG7 2UH, UK1
School of Pharmaceutical Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, UK2
School of Biosciences, University of Nottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK3
Immunology Research, R&D 21, VA Medical Center, Portland, OR 97201, USA4
Author for correspondence: Klaus Winzer. Tel: +44 115 970 9907. Fax: +44 115 970 9923. e-mail: Klaus.Winzer{at}nottingham.ac.uk
Many bacteria produce extracellular molecules which function in cell-to-cell communication. One of these molecules, autoinducer 2 (AI-2), was first described as an extracellular signal produced by Vibrio harveyi to control luciferase expression. Subsequently, a number of bacteria have been shown to possess AI-2 activity in their culture supernatants, and bear the luxS gene product, which is required for AI-2 synthesis. In Porphyromonas gingivalis, luxS and pfs, encoding a 5'-methylthioadenosine/S-adenosylhomocysteine nucleosidase (MTA/SAH’ase), form an operon, suggesting that S-adenosylhomocysteine (SAH) or 5'-methylthioadenosine (MTA) serves as a substrate for AI-2 production. Cell-free extracts of Escherichia coli MG1655, but not DH5
(which carries a luxS frame-shift mutation) were capable of generating AI-2 activity upon addition of SAH, but not MTA. S-Ribosyl-homocysteine (RH) derived from SAH also served as a substrate in E. coli MG1655 extracts. RH-supplemented cell-free extracts of Pseudomonas aeruginosa, a bacterium that lacks luxS, only generated AI-2 activity following the introduction of a plasmid containing the Por. gingivalis pfs-luxS operon. In addition, defined in vitro systems consisting of the purified LuxS proteins from Por. gingivalis, E. coli, Neisseria meningitidis or Staphylococcus aureus converted RH to homocysteine and a compound that exhibits AI-2 activity.4-Hydroxy-5-methyl-3(2H)-furanone was identified by mass spectrometry analysis as a major product formed in this in vitro reaction. In E. coli MG1655, expression of T3SH [the bacteriophage T3 S-adenosylmethionine (SAM) hydrolase] significantly reduced AI-2 activity in culture supernatants, suggesting that AI-2 production is limited by the amount of SAH produced in SAM-dependent transmethylase reactions. The authors suggest that the LuxS protein has an important metabolic function in the recycling of SAH. They also show that Ps. aeruginosa is capable of removing AI-2 activity, implying that this molecule may act as a nutrient. In many bacteria AI-2 may in fact represent not a signal molecule but a metabolite which is released early and metabolized in the later stages of growth.
Keywords: AI-2, S-adenosylhomocysteine, S-ribosylhomocysteine, S-ribosyl-homocysteine-cleavage enzyme, quorum sensing
Abbreviations: AI-2, autoinducer-2; DMHF, 2,5-dimethyl-4-hydroxy-3(2H)-furanone; MTA, 5'-methylthioadenosine; MTA/SAH’ase, 5'-methylthioadenosine/S-adenosylhomocysteine nucleosidase; MHF, 4-hydroxy-5-methyl-3(2H)-furanone; RH, S-ribosylhomocysteine; RLSS, rat liver S-adenosylmethionine synthetase; SAM, S-adenosylmethionine; SAH, S-adenosylhomocysteine; T3SH, bacteriophage T3 SAM hydrolase
a Present address: The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, UK.
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