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Structural identification of a bacterial quorum-sensing signal containing boron

Nature volume 415, pages 545–549 (2002)Cite this article

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 development1,2,3,4. Unlike other autoinducers, which are specific to a particular species of bacteria, a recently discovered autoinducer (AI-2)5 is produced by a large number of bacterial species. AI-2 has been proposed to serve as a ‘universal’ signal for inter-species communication1,2,6,7. 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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Figure 1: The autoinducer AI-2, synthesized by LuxS, is bound by the sensor protein LuxP.
Figure 2: Structure of LuxP-AI-2 complex.
Figure 3: Structure of AI-2.
Figure 4: Synthesis of AI-2 from DPD and borate.

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Acknowledgements

We acknowledge S. Cooper for suggesting that AI-2 could be a cyclic borate diester. We thank R. Carroll, M. Case, S. Miller, K. Xavier and A. Saxena and the staff of the National Synchrotron Light Source beamline X12C for technical assistance, and J. Carey, C. Eckhert, D. Kahne, C. Lee, Y. Shi, K. Shokat, T. Silhavy, and members of the Hughson and Bassler laboratories for discussions. This research was supported by a Deutsche Academischer Austaschdienst (DAAD) fellowship (S.S.), NSF and the Office of Naval Research (ONR) (B.L.B.), and NIH (F.M.H.).

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Authors and Affiliations

  1. Department of Molecular Biology, Princeton University, Princeton, USA, 08544-1014, New Jersey

    Xin Chen, Stephan Schauder, Bonnie L. Bassler & Frederick M. Hughson

  2. Department of Chemistry, Princeton University, Princeton, 08544-1014, New Jersey, USA

    István Pelczer

  3. Laboratoire de Spectrometrie de Masse Bio-Organique, Ecole de Chimie, Polymeres et Materiaux, 25 Rue Becquerel, Strasbourg, 67087, France

    Noelle Potier & Alain Van Dorsselaer

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  1. Xin Chen
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  2. Stephan Schauder
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Correspondence to Frederick M. Hughson.

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Chen, X., Schauder, S., Potier, N. et al. Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415, 545–549 (2002). https://doi.org/10.1038/415545a

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