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AUTOINDUCER 2, Luxs and PATHOGENIC BACTERIA

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AUTOINDUCER 2, Luxs and PATHOGENIC BACTERIA REVIEWS MAKING ‘SENSE’ OF METABOLISM: AUTOINDUCER2, LuxS AND PATHOGENIC BACTERIA Agnès Vendeville*, Klaus Winzer‡, Karin Heurlier‡, Christoph M. Tang* and Kim R. Hardie‡ Abstract | Bacteria exploit many mechanisms to communicate with each other and their surroundings. Mechanisms using small diffusible signals to coordinate behaviour with cell density (quorum sensing) frequently contribute to pathogenicity. However, pathogens must also be able to acquire nutrients and replicate to successfully invade their host. One quorum-sensing system, based on the possession of LuxS, bears the unique feature of contributing directly to metabolism, and therefore has the potential to influence both gene regulation and bacterial fitness. Here, we discuss the influence that LuxS and its product, autoinducer-2, have on virulence, relating the current evidence to the preferred niche of the pathogen and the underlying mechanisms involved. BIOFILM In most environmental niches, bacteria exist in phenomenon whereby the accumulation of specific, Complex population of complex communities of single or multiple species diffusible, low-molecular-weight signal molecules (or organisms on a surface. that develop on abiotic (for example, rocks) or biotic ‘autoinducers’) enables bacteria to sense when the (for example, host mucosal tissues) surfaces1–3 rather minimal number, or ‘quorum’, of bacteria has been than as single, planktonic cells suspended in liquid. achieved for a concerted response to be initiated5–7. As such niches are diverse, microorganisms depend Both Gram-negative and Gram-positive pathogens on their capacity to sense the local environmental are known to use autoinducer molecules to coordi- conditions and adapt by regulating the expression of nate expression of genes crucial for virulence and *Centre for Molecular specific genes. This is particularly vital for pathogenic survival. Delaying virulence factor production until Microbiology and Infection, bacteria, which encounter a range of habitats in a a certain population density is reached might allow Department of Infectious host. Consequently, bacteria have developed several for a host to be overwhelmed before its innate Diseases, Faculty of Medicine, Flowers Building, highly sophisticated mechanisms to gather, process immune response is fully activated. In addition, this Armstrong Road, Imperial and transduce environmental information such as process might enable bacteria to function in concert College London, London pH, temperature, nutrient availability, osmolarity and with the characteristics of a multicellular organism SW7 2AZ, UK. cell population density. Many different signal trans- by acquiring an organization such as a BIOFILM, which ‡ Institute of Infection, duction mechanisms in bacteria control the synthesis can aid either pathogenesis or the establishment of Immunity, and 8 Inflammation, Centre for of colonization factors, toxins and tissue-degrading specific symbiotic associations with eukaryotic hosts . Biomolecular Sciences, enzymes, which might only be necessary in specific The production of autoinducers might also facilitate Nottingham University, host compartments and detrimental to the bacterium the detection of a diffusion barrier or compartment Nottingham, NG7 2RD, UK. in others4. boundary9,10. Correspondence to K.R.H. e-mail: kim.hardie@ Many bacteria secrete small, diffusible, signalling Among the many different mechanisms for quorum 7 nottingham.ac.uk molecules. It is generally assumed that these molecules sensing that have evolved , the most-characterized doi:10.1038/nrmicro1146 are used for a process termed ‘quorum sensing’, the quorum-sensing systems involve the production of NATURE REVIEWS | MICROBIOLOGY VOLUME 3 | MAY 2005 | 383 © 2005 Nature Publishing Group REVIEWS LsrB ligand Toxic metabolite LuxP ligand Here, we discuss the physiology of AI-2 production –2H O 2 HO – OH HO OH – and sensing by bacteria, and the relationship between HO CH3 HO CH3 +B(OH)4 B HO OH HO CH3 O O LuxS and the AMC. Furthermore, we review the recent O O O HO CH3 data on the impact of LuxS on the pathogenesis of HO O HO O HO human infections. R-THMF MHF S-THMF S-THMF-borate LuxS and AI-2 –H O–HO H2O H2O 2 2 Formation of AI-2. AI-2 is a byproduct of the AMC (FIG. 1), which recycles SADENOSYLLMETHIONINE (SAM), OH O CH3 O the main methyl donor in eubacterial, archaebacterial OH CH3 and eukaryotic cells. As part of the AMC, SAM is con- O O HO HO verted to SADENOSYLLHOMOCYSTEINE (SAH), which is R-DHMF S-DHMF subsequently detoxified by the Pfs enzyme (also called OH O 5'-methyl thioadenosine/S-adenosylhomocysteine Activated methyl cycle nucleosidase) to generate adenine and the sole intra- OH O Pfs SRH SAH X-CH3 cellular source of the substrate of LuxS, SRIBOSYL DPD HOMOCYSTEINE LuxS X (SRH). LuxS then produces the precursor of AI-2, 4,5DIHYDROXY2,3PENTANEDIONE DPD, during the SahH conversion of SRH to HOMOCYSTEINE (HCY)8,20. Many Oxaloacetate HCY SAM organisms, in particular eukaryotes, replace this two- MetB step process with a single enzyme, SAH hydrolase CysK (SahH), which converts SAH to homocysteine without 2– 2– SO4 S CYS MET producing AI-2 REFS 20,21. Figure 1 | Chemical interconversions of molecules in relation to the activated methyl cycle. The reactions that generate homocysteine (HCY) from (i) sulphate (SO 2–) through Biochemistry of the reaction catalysed by LuxS. The 4 22–24 sulphide (S2–), and (ii) oxaloacetate (OA), plus some of the enzymes involved (MetB and CysK) are available crystal structures of LuxS homologues shown feeding into the boxed reactions that comprise the activated methyl cycle (shaded in light depict a homodimer with a fold that is unique to a blue). The latter involves the formation of methione (MET) and the subsequent conversion to small family of enzymes with related functions. Two S-adenosylmethionine (SAM). The activated methyl group (CH ) of SAM is used for methylation 3 identical active sites are formed at the dimer interface of RNA, DNA, certain metabolites and proteins (X), leading to the formation of the toxic by residues from both subunits contained within the metabolite S-adenosylhomocysteine (SAH). SAH is then removed and the cycle completed by invariant HXXEH motif, where an Fe2+ ion is tetra- one of two routes, depending on the organism. One route involves the one-step conversion of SAH to HCY by SAH hydrolase (SahH), the other requires the production of hedrally coordinated. To achieve the predicted chemical S-ribosylhomocysteine (SRH) by Pfs and then the generation of HCY from this by LuxS, which conversion, it is proposed that a series of proton- simultaneously generates 4,5-dihydroxy-2,3-pentanedione (DPD). There is spontaneous transfer reactions occurs, catalysed by the Fe2+ ion25 cyclization of DPD to either the R or S form of 2,4-dihydroxy-2-methyldihydro-3-furanone and two residues of LuxS26. These properties identify (DHMF). R-DHMF can then undergo hydration to form the molecule which was co-crystalized LuxS as the previously described ribosylhomocysteine- with LsrB, (2R,4S)-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran (R-THMF, red box). cleavage enzyme27,28 shown to be responsible for DPD Alternatively, hydrolysis can occur to create 4-hydroxy-5-methyl-3(2H)-furanone (MHF, yellow box). MHF can also be formed through hydrolysis of S-DHMF, which can additionally undergo formation in Escherichia coli (for more detailed over- hydration to form S-THMF and subsequently form a diester with boric acid to generate the ligand views of LuxS structure and catalysis see REFS 19,29). found in complex with LuxP (green box). Where known, the reversible nature of interconversions are indicated by the double arrows. Based on data from REFS 19,28,31. The chemical nature of AI-2. Although DPD is the molecule synthesized alongside HCY by LuxS, AI-2 activity is associated with cyclic derivatives of this ACTIVATED METHYL CYCLE N-acyl-l-homoserine lactones (AHLs) by Gram- molecule that can be generated spontaneously30,31. Metabolic cycle which negative bacteria6,11,12. AHLs are usually produced by The chemical structures first attributed to AI-2 activity generates the methyl donor S-adenosyl-l-methionine and a protein homologous to LuxI, but can be generated were furanone derivatives (particularly 4HYDROXY5 13–16 recycles methionine through by other enzymes . Signalling through the production METHYL32HFURANONE, MHF), by virtue of their ability S-adenosyl homocysteine and of post-translationally modified peptides is confined to to induce bioluminescence in the Vibrio harveyi bio- homocysteine. S-adenosyl-l- Gram-positive bacteria17. assay20,32. Although it can activate the V. har vey i biosen- methionine provides activated methyl groups for use in the The only quorum-sensing mechanism shared by sor and is the main product present in methanol methylation of proteins, RNA, both Gram-positive and Gram-negative bacteria extracts of the in vitro AI-2 synthetic reaction mixture, DNA and certain metabolites. involves the production of autoinducer 2 (AI-2) by MHF (which can be derived from DPD, see FIG. 1) the enzyme LuxS8,18. This pathway is found in over showed lower activity than AI-2, which indicates that SADENOSYLLMETHIONINE 55 species, leading to the suggestion that AI-2 is a there is at least one other molecule in LuxS in vitro Important methyl 18 donor in the cell. universal language for interspecies communication . reaction mixtures with a higher activity than However, LuxS has an alternative role in the cell, in MHF19,20,32. The finding that more than one molecule SADENOSYLL which it functions as an integral component of the can behave as AI-2 initiated the use of ‘AI-2’ as a col- HOMOCYSTEINE ACTIVATED METHYL CYCLE (AMC)19. This link could also lective term, a practise that was required after the Produced from S-adenosyl- l-methionine following the provide an explanation for the widespread conserva- discovery of further DPD-derived molecules found release of methyl groups tion of luxS, although further investigation is required in complex with two AI-2-binding proteins following by methyltransferases.
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