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September 18, 2002 Structural Identification of a Bacterial Quorum Sensing Signal Containing BoronX. Chen1, S. Schauder1, I. Pelczer1, L. Bassler1, F.M. Hughson1, N. Potier2, and A. Van Dorsselaer2 In a process known as quorum sensing, bacteria communicate with one another using chemical signalling molecules called autoinducers. This cell-cell communication allows a population of bacteria to coordinate the gene expression, and therefore the behavior, of the group. Recent work by researchers from Princeton University and the School of Chemistry, Polymers and Materials in Strasbourg, France, has led to the identification of a novel autoinducer, AI-2, that may serve as a ‘universal’ signal for communication between different bacterial species. AI-2 unexpectedly contains boron, an element that, while ubiquitous in the biosphere, has seldom been observed to play a role in biological processes.
Recently, we identified a novel autoinducer, AI-2, that has the potential to mediate communication among different bacterial species. The presence of AI-2 can be detected by adding it to a specially engineered strain of the bioluminescent marine bacterium V. harveyi, which emits light in the presence of AI-2. Using this assay, it was possible to show that a large number of bacterial species produce AI-2. These and other findings suggest that communication via AI-2 could be a common mechanism that bacteria employ for inter-species interaction in natural environments. The chemical identity of AI-2 was ascertained in a somewhat unusual way using x-ray crystallography. AI-2 was crystallized in a complex with its V. harveyi receptor protein, LuxP. Crystals formed by the LuxP-AI-2 complex diffracted beyond 1.5 Å resolution at NSLS Beamline X-12C. Because of the high quality of the resulting electron density maps, it was straightforward to construct an atomic model for AI-2 (Figure 1).
Earlier work had suggested that AI-2 is derived from the precursor 4,5-dihydroxy-2,3-pentanedione. The cyclic form of this precursor is a plausible substrate for the addition of borate. We were nonetheless surprised to find that the AI-2 electron density appears to match this borate addition product. Confirmatory evidence, including 11B-NMR spectra and the ability of boric acid to stimulate bioluminescence in V. harveyi supported the conclusion that AI-2 is a novel furanosyl borate diester. Thus, interspecies quorum sensing represents one of the first biochemically defined roles for boron in biology. Many questions remain. For example, it is not yet clear how, or whether, the use of boron enhances signal transmission or signal specificity. Also, we do not yet know whether the use of boron in cell-cell signaling is confined to bacteria that live in marine environments or is more widespread. Nonetheless, biotechnological research is focused on the development of molecules that are structurally related to AI-2. Such molecules may be useful as anti-microbial drugs aimed at bacteria that control virulence through AI-2 quorum sensing. Since many bacteria produce AI-2, drugs that target AI-2 quorum sensing could be broadly used in the future. FUNDING PUBLICATION FOR MORE INFORMATION |
The National Synchrotron Light Source at Brookhaven National Laboratory in New York, is a national user research
facility funded by the U.S. Department of Energy's Office of Basic Energy Science. The NSLS operates two electron
storage rings: an X-Ray ring and a Vacuum UltraViolet (VUV) ring which provide intense light spanning the electromagnetic
spectrum from the infrared through x-rays. Each year over 2300 scientists from universities, industries and government
labs perform research at the NSLS.
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Quorum sensing allows a population of bacteria to coordinate
their gene expression, and therefore their collective behavior.
Usually, quorum sensing controls processes that are effective when a
large number of bacteria act together. Some bacteria, for example,
produce visible light in response to autoinducers that accumulate in
dense cultures. Pathogenic bacteria can use quorum sensing to evade
the immune system, express toxic virulence factors, or coordinate
the formation of antibiotic-resistant biofilms.