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Bacterial Attraction and Quorum Sensing Inhibition in Caenorhabditis elegans Exudates

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Abstract

Caenorhabditis elegans, a bacterivorous nematode, lives in complex rotting fruit, soil, and compost environments, and chemical interactions are required 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 signals that C. elegans uses to interact chemically with its environment or as defense. C. elegans exudates were analyzed by using several analytical methods and found to contain 36 common metabolites that include organic acids, amino acids, and sugars, all in relatively high abundance. Furthermore, the concentrations of amino acids in the exudates were dependent on developmental stage. The C. elegans exudates were tested for bacterial chemotaxis using Pseudomonas putida (KT2440), a plant growth promoting rhizobacterium, Pseudomonas aeruginosa (PAO1), a soil bacterium pathogenic to C. elegans, and Escherichia coli (OP50), a non-motile bacterium tested as a control. The C. elegans exudates attracted the two Pseudomonas species, but had no detectable antibacterial activity against P. aeruginosa. To our surprise, the exudates of young adult and adult life stages of C. elegans exudates inhibited quorum sensing in the reporter system based on the LuxR bacterial quorum sensing (QS) system, which regulates bacterial virulence and other factors in Vibrio fischeri. We were able to fractionate the QS inhibition and bacterial chemotaxis activities, thus demonstrating that these activities are chemically distinct. Our results demonstrate that C. elegans can attract its bacterial food and has the potential of partially regulating the virulence of bacterial pathogens by inhibiting specific QS systems.

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Acknowledgement

Funding was provided through the Human Frontier Science Program (ASE), the NIH (1R01GM085285-01 to ASE), the NSF (MCB-0429968 to SR), and the NSF funded National High Magnetic Field Laboratory (DMR-0654118). We thank Dr Michael Givskov for providing the GFP-based AHL sensor system and QSIS1 reporter system. We thank Drs. Paul Sternberg and Jagan Srinivasan for helping to establish biological activity of worm water and Drs. David Powell, Mario de Bono, Frank Schroeder, and Peter Teal for helpful ideas in the worm water protocol and Alex K. Brasher for his help collecting worm exudates. NMR data were collected in the University of Florida AMRIS Facility, and we thank Jim Rocca for his help with NMR data collection and interpretation.

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Authors and Affiliations

  1. Center for Medical, Agricultural and Veterinary Entomology, USDA-ARS, Gainesville, FL, USA

    Fatma Kaplan & Hans T. Alborn

  2. Center for Rhizosphere Biology, Colorado State University, Fort Collins, CO, USA

    Dayakar V. Badri & Jorge M. Vivanco

  3. Department of Biochemistry & Molecular Biology, University of Florida, Gainesville, FL, USA

    Cherian Zachariah, Ramadan Ajredini, Steven L. Robinette, Michael Stadler, Rathika Nimalendran, Aaron T. Dossey & Arthur S. Edison

  4. National High Magnetic Field Laboratory, University of Florida, Gainesville, FL, USA

    Cherian Zachariah, Ramadan Ajredini, Steven L. Robinette, Michael Stadler, Rathika Nimalendran, Aaron T. Dossey & Arthur S. Edison

  5. McKnight Brain Institute, University of Florida, Gainesville, FL, USA

    Cherian Zachariah, Ramadan Ajredini, Steven L. Robinette, Michael Stadler, Rathika Nimalendran, Aaron T. Dossey & Arthur S. Edison

  6. Institute of Biological Chemistry, Washington State University, Pullman, WA, USA

    Francisco J. Sandoval & Sanja Roje

  7. Dynamac Corporation, Kennedy Space Center, Brevard County, FL, USA

    Lanfang H. Levine

  8. National High Magnetic Field Laboratory and Dept of Chemistry, Florida State University, Tallahassee, FL, USA

    Fengli Zhang & Rafael Brüschweiler

  9. St. Jude Children’s Research Hospital, Memphis, TN, USA

    Wei Zhao

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  1. Fatma Kaplan
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Corresponding author

Correspondence to Arthur S. Edison.

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Author contributions

Fatma Kaplan and Dayakar V. Badri contributed equally and led the study; Fatma Kaplan, Aaron T. Dossey, Ramadan Ajredini, Hans Alborn and Michael Stadler intellectually contributed to the worm exudate protocol which was developed in the ASE laboratory; Fatma Kaplan, Ramadan Ajredini, and Rathika Nimalendran collected exudates; Dayakar V. Badri conducted bacterial bioassays; Hans Alborn collected LC-MS data; Fatma Kaplan and Cherian Zachariah collected NMR data; Fengli Zhang, Steven L. Robinette and Rafael Brüschweiler did COLMAR analysis; Fatma Kaplan, Cherian Zachariah, Michael Stadler, and Aaron T. Dossey manually analyzed NMR data. Sanja Roje and Francisco Sandoval analyzed amino acids by HPLC; Lanfang H. Levine analyzed young adult exudates by GC-MS; Wei Zhao did principle component analysis; Fatma Kaplan, Dayakar V. Badri, Arthur S. Edison and Jorge M. Vivanco analyzed the data and wrote the paper with help from the entire team.

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Kaplan, F., Badri, D.V., Zachariah, C. et al. Bacterial Attraction and Quorum Sensing Inhibition in Caenorhabditis elegans Exudates. J Chem Ecol 35, 878–892 (2009). https://doi.org/10.1007/s10886-009-9670-0

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  • DOI: https://doi.org/10.1007/s10886-009-9670-0

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