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PLANTS INTERACTING WITH OTHER ORGANISMS

Chlamydomonas reinhardtii Secretes Compounds That Mimic Bacterial Signals and Interfere with Quorum Sensing Regulation in Bacteria¹

ARC Centre of Excellence for Integrative Legume Research Genomics Interaction Group, Research School of Biological Sciences, Australian National University, Canberra, Australian Capitol Territory 2601, Australia (H.C., B.G.R.); Graduate Program in Biophysics (S.R., R.T.S.) and Departments of Plant Pathology (M.M.) and Plant Biology (R.T.S.), Ohio State University, Columbus, Ohio 43210 (M.T., M.G., W.D.B.); and Department of Biology, University of Dayton, Dayton Ohio 45469 (J.B.R.)

The unicellular soil-freshwater alga Chlamydomonas reinhardtii was found to secrete substances that mimic the activity of the N-acyl-L-homoserine lactone (AHL) signal molecules used by many bacteria for quorum sensing regulation of gene expression. More than a dozen chemically separable but unidentified substances capable of specifically stimulating the LasR or CepR but not the LuxR, AhyR, or CviR AHL bacterial quorum sensing reporter strains were detected in ethyl acetate extracts of C. reinhardtii culture filtrates. Colonies of C. reinhardtii and Chlorella spp. stimulated quorum sensing-dependent luminescence in Vibrio harveyi, indicating that these algae may produce compounds that affect the AI-2 furanosyl borate diester-mediated quorum sensing system of Vibrio spp. Treatment of the soil bacterium Sinorhizobium meliloti with a partially purified LasR mimic from C. reinhardtii affected the accumulation of 16 of the 25 proteins that were altered in response to the bacterium's own AHL signals, providing evidence that the algal mimic affected quorum sensing-regulated functions in this wild-type bacterium. Peptide mass fingerprinting identified 32 proteins affected by the bacterium's AHLs or the purified algal mimic, including GroEL chaperonins, the nitrogen regulatory protein PII, and a GTP-binding protein. The algal mimic was able to cancel the stimulatory effects of bacterial AHLs on the accumulation of seven of these proteins, providing evidence that the secretion of AHL mimics by the alga could be effective in disruption of quorum sensing in naturally encountered bacteria.

¹ This work was supported by the U.S. Department of Agriculture National Research Initiatives (grant no. 2002-3531911559 to B.G.R., J.B.R., and W.D.B.), by the Ohio Plant Biotechnology Consortium (grant no. to J.B.R. and W.D.B), by the Ohio State University Office of International Education Travel (grants to W.D.B and M.T.), by the Ohio Agricultural Research and Development Center (presidential fellowship to M.T.), by the Ohio State University (Research Enhancement grant and Extension Sustainable Agriculture grant to M.T.), and by state and federal funds appropriated to the Ohio Agricultural Research and Development Center in partial salary and research support to W.D.B. This is contribution no. 03-14 of Department of Horticulture and Crop Science.

² Present address: Department of Microbiology, Ohio State University, 484 W. 12th Avenue, Columbus, OH 43210.

^* Corresponding author; e-mail bauer.7{at}osu.edu; fax 614-292-9035.

Received July 14, 2003; returned for revision August 4, 2003; accepted September 15, 2003.

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