A new class of homoserine lactone quorum-sensing signals

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Abstract

Quorum sensing is a term used to describe cell-to-cell communication that allows cell-density-dependent gene expression. Many bacteria use acyl-homoserine lactone (acyl-HSL) synthases to generate fatty acyl-HSL quorum-sensing signals, which function with signal receptors to control expression of specific genes. The fatty acyl group is derived from fatty acid biosynthesis and provides signal specificity, but the variety of signals is limited. Here we show that the photosynthetic bacterium Rhodopseudomonas palustris uses an acyl-HSL synthase to produce p-coumaroyl-HSL by using environmental p-coumaric acid rather than fatty acids from cellular pools. The bacterium has a signal receptor with homology to fatty acyl-HSL receptors that responds to p-coumaroyl-HSL to regulate global gene expression. We also found that p-coumaroyl-HSL is made by other bacteria including Bradyrhizobium sp. and Silicibacter pomeroyi. This discovery extends the range of possibilities for acyl-HSL quorum sensing and raises fundamental questions about quorum sensing within the context of environmental signalling.

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Figure 1: The rpaI gene has potential RpaR binding sites in its promoter and plant-derived aromatic acids activate its expression.
Figure 2: Evidence indicating that the R. palustris quorum-sensing signal is p C-HSL.
Figure 3: p C-HSL is made during growth, requires RpaR for quorum-sensing-dependent activity, is synthesized by RpaI, and is made by other bacteria.

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Primary accessions

Gene Expression Omnibus

Data deposits

The primary microarray data have been deposited in the NCBI’s Gene Expression Omnibus (GEO, http://www.ncbi.nlm.nih.gov/geo) under the accession number GSE10642.

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Acknowledgements

We thank B. Howald and R. Lawrence for their expertise in MS analyses, and W. Tabaczynski for his expertise in NMR analysis. This work was supported by the US Army Research Office, US Department of Energy (C.S.H.), and the National Institute of General Medical Sciences (E.P.G.). C.M.O. was supported by a National Cancer Institute Training Grant.

Author Contributions A.L.S. performed all experiments except those described below. C.M.O. and J.R.S. performed and interpreted NMR analyses and synthesized pC-HSL. Y.O. assisted in substrate survey and growth curve experiments and performed RT–PCR analyses. J.J.H. constructed strains and performed experiments analysing RpaR-dependent gene activation. G.B.-B. and C.M.P. constructed strains. S.S. purified MBP–RpaI protein. K.J. synthesized p-coumaroyl-CoA. A.L.S., E.P.G. and C.S.H. designed experiments, analysed data and wrote the paper.

Author information

Correspondence to Caroline S. Harwood.

Supplementary information

Supplementary Information

This file contains the multiple alignments of LuxI-R family members with RpaI-R (Supplementary Fig. 1), structures of aromatic acid substrates surveyed for signal production (Supplementary Fig. 2), NMR analysis of the R. palustris quorum sensing signal (Supplementary Fig. 3), and a table of those genes controlled by pC-HSL (Supplementary Table 1). (PDF 1528 kb)

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