Structural identification of a bacterial quorum-sensing signal containing boron

Abstract

Cell-cell communication in bacteria is accomplished through the exchange of extracellular signalling molecules called autoinducers. This process, termed quorum sensing, allows bacterial populations to coordinate gene expression. Community cooperation probably enhances the effectiveness of processes such as bioluminescence, virulence factor expression, antibiotic production and biofilm development. Unlike other autoinducers, which are specific to a particular species of bacteria, a recently discovered autoinducer (AI-2) is produced by a large number of bacterial species. AI-2 has been proposed to serve as a 'universal' signal for inter-species communication. The chemical identity of AI-2 has, however, proved elusive. Here we present the crystal structure of an AI-2 sensor protein, LuxP, in a complex with autoinducer. The bound ligand is a furanosyl borate diester that bears no resemblance to previously characterized autoinducers. Our findings suggest that addition of naturally occurring borate to an AI-2 precursor generates active AI-2. Furthermore, they indicate a potential biological role for boron, an element required by a number of organisms but for unknown reasons.

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“…Cells were once thought incapable of processing the element, yet this has since been disproved. Boron is utilised by bacteria in the structure of several antibiotics and autoinducer-2, a signalling molecule utilised during interspecies quorum sensing (Chen et al, 2002;Semmelhack et al, 2004). Plants require the element for growth, flowering and seed formation, and obtain boron from soil pore water using a borate transporter, BOR1, expressed in root pericycle cells (Takano et al, 2002).…”

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“…The catalytic process of LuxS involves the fragmentation of a byproduct of SAM metabolism, (S) -ribosyl-homocysteine (SRH), to produce homocysteine and the AI-2 precursor, 4,5-dihydroxy-2,3-pentanedione (DPD). DPD spontaneously cyclizes and borate is chelated to yield AI-2, identified as (2S,4S)-2-methyl-2,3,4-tetrahydroxytetrahydrofuran-borate [41,42]. The CAI-1 (Cholera Autoinducer-1), a stronger signal, was previously identified as (S)-3-hydroxytridecan-4-one known to require the enzyme CqsA for its biosynthesis [33,43].…”

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“…Since then, researchers have observed this 'quorum-sensing' behaviour in many species [2][3][4] and have started to decipher the biochemistry and genetics of how it happens 5 . They have also been developing devices with which to characterize the messages that are transmitted and received.…”