Bacterial attraction and quorum sensing inhibition in Caenorhabditis elegans exudates

Authors: KAPLAN, FATMA - UF, BIOCHEMISTRY AND MOLE; BADRI, DAYAKAR - COLORADO STATE UNIVERSITY; ZACHARIAH, CHERIAN - UF, BIOCHEMISTRY AND MOLE; AJREDINI, RAMAZAN - UF, BIOCHEMISTRY AND MOLE; SANDOVAL, FRANCISCO - WASHINGTON STATE UNIVERSI; ROJE, SANJA - WASHINGTON STATE UNIVERSI; LEVINE, LANFANG - KENNEDY SPACE CENTER,FL; ZHANG, FENGLI - FLORIDA STATE UNIVERSITY; ROBINETTE, STEVE - UF, BIOCHEMISTRY AND MOLE; Alborn, Hans; ZHAO, WEI - ST. JUDE CHILDREN'S RESEA; STADLER, MIKE - UF, BIOCHEMISTRY AND MOLE; NIMALENDRAN, RATHIKA - UF, BIOCHEMISTRY AND MOLE; DOSSEY, AARON - UF, BIOCHEMISTRY AND MOLE; BRUSCHWEILER, RAFAEL - FLORIDA STATE UNIVERSITY; VIVANCO, JORGE - COLORADO STATE UNIVERSTY; EDISON, ARTHUR - UF, BIOCHEMISTRY AND MOLE

Submitted to: Journal of Chemical Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/9/2009
Publication Date: 7/4/2009
Citation: Kaplan, F., Badri, D.V., Zachariah, C., Ajredini, R., Sandoval, F.J., Roje, S., Levine, L.H., Zhang, F., Robinette, S.L., Alborn, H.T., Zhao, W., Stadler, M., Nimalendran, R., Dossey, A.T., Bruschweiler, R., Vivanco, J.M., Edison, A.S. 2009. Bacterial attraction and quorum sensing inhibition in Caenorhabditis elegans exudates. Journal of Chemical Ecology. 35:878-892.

Interpretive Summary: Despite that the nematode Caenorhabditis elegans is one of the best-studied model organisms in biology, little is known about how it interacts chemically with its environment. In a multidisciplinary collaboration within several research groups, a scientist at USDA ARS, CMAVE in Gainesville studied the composition of C. elegans exudates and investigated their effect on soil bacteria. The exudates, which contain a variety of sugars, organic acids, and amino acids, were shown to attracted bacterial species, including species pathogenic to C. elegans. However, the nematodes were shown also to also produce one or more developmentally regulated inhibitors of bacterial quorum sensing (QS) which, among other things, regulates bacterial virulence. This suggests that C. elegans has evolved as a mechanism to survive pathogenic species of bacteria without employing antibiotics and that C. elegans plays an active role in soil chemical ecology and may even have evolved a system for “bacterial farming”; effectively attracting and promoting growth of its own food source. This research is likely to have implications also for agriculture; by understanding the chemical signaling and behavior of C. elegans we might find ways to manipulate or control the behavior of considerably more important soil bound phytophagous nematodes.

Technical Abstract: Caenorhabditis elegans, a bacterivorous soil nematode, lives in a complex environment that requires chemical communication for mating, monitoring population density, recognition of food, avoidance of pathogenic microbes, and other essential ecological functions. Despite being one of the best-studied model organisms in biology, relatively little is known about the chemical signals that C. elegans uses for communication with its environment or defense. This study demonstrates that water soluble C. elegans exudates called worm water (WW), collected at several key developmental stages, contain at least 36 common metabolites including organic acids, amino acids and sugars, all in relatively high abundance. Many of these compounds are known to attract bacteria, and Pseudomonas putida, a plant growth promoting rhizobacteria and Pseudomonas aeruginosa, a soil bacterium pathogenic to C. elegans, were attracted to C. elegans WW. Furthermore, C. elegans WW had no antibacterial activity against P. aeruginosa at any life stage. To our surprise, the WW inhibited bacterial quorum sensing (QS), which regulates bacterial virulence and other factors. This QS inhibition was developmentally regulated and active only at young adult and adult life stages.