Journal of Chemical Ecology

, Volume 35, Issue 8, pp 878–892 | Cite as

Bacterial Attraction and Quorum Sensing Inhibition in Caenorhabditis elegans Exudates

  • Fatma Kaplan
  • Dayakar V. Badri
  • Cherian Zachariah
  • Ramadan Ajredini
  • Francisco J. Sandoval
  • Sanja Roje
  • Lanfang H. Levine
  • Fengli Zhang
  • Steven L. Robinette
  • Hans T. Alborn
  • Wei Zhao
  • Michael Stadler
  • Rathika Nimalendran
  • Aaron T. Dossey
  • Rafael Brüschweiler
  • Jorge M. Vivanco
  • Arthur S. Edison
Article

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.

Keywords

C. elegans exudates Bacterial chemotaxis Metabolomics Quorum sensing inhibitor Chemical ecology Nematodes 

Supplementary material

10886_2009_9670_MOESM1_ESM.doc (363 kb)
Supplementary material(DOC 363 kb)

References

  1. ABALLAY, A., and AUSUBEL, F. M. 2002. Caenorhabditis elegans as a host for the study of host-pathogen interactions. Curr. Opin. Microbiol. 5:97–101.PubMedCrossRefGoogle Scholar
  2. ADLER, J. 1966. Chemotaxis in bacteria. Science. 153:708–716.PubMedCrossRefGoogle Scholar
  3. ADLER, J., HAZELBAUER, G. L., and DAHL, M. M. 1973. Chemotaxis toward sugars in Escherichia coli. J. Bacteriol. 115:824–847.PubMedGoogle Scholar
  4. ANDERSEN, J. B., HEYDORN, A., HENTZER, M., EBERL, L., GEISENBERGER, O., CHRISTENSEN, B. B., MOLIN, S., and GIVSKOV, M. 2001. gfp-based N-acyl homoserine-lactone sensor systems for detection of bacterial communication. Appl. Environ. Microbiol. 67:575–585.PubMedCrossRefGoogle Scholar
  5. AVERY, L., and SHTONDA, B. B. 2003. Food transport in the C. elegans pharynx. J. Exp. Biol. 206:2441–2457.PubMedCrossRefGoogle Scholar
  6. BACILIO-JIMÉNEZ, M., AGUILAR-FLORES, S., VENTURA-ZAPATA, E., PEREZ-CAMPOS, E., BOUQUELET, S., and ZENTENO, E. 2003. Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant and Soil. 249:271–277.CrossRefGoogle Scholar
  7. BAIS, H. P., PRITHIVIRAJ, B., JHA, A. K., AUSUBEL, F. M., and VIVANCO, J. M. 2005. Mediation of pathogen resistance by exudation of antimicrobials from roots. Nature. 434:217–221.PubMedCrossRefGoogle Scholar
  8. BARRIERE, A., and FELIX, M. A. 2006. Isolation of C. elegans and related nematodes. WormBook. 1–9.Google Scholar
  9. BAUER, A. W., KIRBY, W. M., SHERRIS, J. C., and TURCK, M. 1966. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 45:493–496.PubMedGoogle Scholar
  10. BEALE, E., LI, G., TAN, M. W., and RUMBAUGH, K. P. 2006. Caenorhabditis elegans senses bacterial autoinducers. Appl. Environ. Microbiol. 72:5135–5137.PubMedCrossRefGoogle Scholar
  11. BERTANI, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62:293–300.PubMedGoogle Scholar
  12. BJARNSHOLT, T., and GIVSKOV, M. 2007. Quorum-sensing blockade as a strategy for enhancing host defences against bacterial pathogens. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362:1213–1222.PubMedCrossRefGoogle Scholar
  13. BRENNER, S. 1974. Genetics of Caenorhabditis elegans. Genetics. 77:71–94.PubMedGoogle Scholar
  14. BREY, W. W., EDISON, A. S., NAST, R. E., ROCCA, J. R., SAHA, S., and WITHERS, R. S. 2006. Design, construction, and validation of a 1-mm triple-resonance high-temperature-superconducting probe for NMR. J. Magn. Reson. 179:290–293.PubMedCrossRefGoogle Scholar
  15. BRÜSCHWEILER, R., and ZHANG, F. 2004. Covariance nuclear magnetic resonance spectroscopy. J. Chem. Phys. 120:5253–5260.PubMedCrossRefGoogle Scholar
  16. BUTCHER, R. A., FUJITA, M., SCHROEDER, F. C., and CLARDY, J. 2007. Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat. Chem. Biol. 3:420–422.PubMedCrossRefGoogle Scholar
  17. BUTCHER, R. A., RAGAINS, J. R., KIM, E., and CLARDY, J. 2008. A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components. Proc. Natl. Acad. Sci. U. S. A. 105:14288–14292.PubMedCrossRefGoogle Scholar
  18. CHALFIE, M., TU, Y., EUSKIRCHEN, G., WARD, W. W., and PRASHER, D. C. 1994. Green fluorescent protein as a marker for gene expression. Science. 263:802–805.PubMedCrossRefGoogle Scholar
  19. CLARK, D. J., and MAAOLE, O. 1967. DNA replication and the division cycle in Escherichia coli. J. Mol. Biol. 23:99–112.CrossRefGoogle Scholar
  20. COHEN, S. A., and MICHAUD, D. P. 1993. Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for the analysis of hydrolysate amino acids via high-performance liquid chromatography. Anal. Biochem. 211:279–287.PubMedCrossRefGoogle Scholar
  21. DARBY, C., COSMA, C. L., THOMAS, J. H., and MANOIL, C. 1999. Lethal paralysis of Caenorhabditis elegans by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 96:15202–15207.PubMedCrossRefGoogle Scholar
  22. DELAGLIO, F., GRZESIEK, S., VUISTER, G. W., ZHU, G., PFEIFER, J., and BAX, A. 1995. NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR. 6:277–293.PubMedCrossRefGoogle Scholar
  23. DONG, Y. H., WANG, L. Y., and ZHANG, L. H. 2007. Quorum-quenching microbial infections: mechanisms and implications. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362:1201–1211.PubMedCrossRefGoogle Scholar
  24. ELLIS, R. E., YUAN, J. Y., and HORVITZ, H. R. 1991. Mechanisms and Functions of Cell-Death. Annu. Rev. Cell Biology. 7:663–698.Google Scholar
  25. FIEHN, O., KOPKA, J., DÈORMANN, P., ALTMANN, T., TRETHEWEY, R. N., and WILLMITZER, L. 2000. Metabolite profiling for plant functional genomics. Nat. Biotechnol. 18:1157–1161.PubMedCrossRefGoogle Scholar
  26. FIRE, A., XU, S. Q., MONTGOMERY, M. K., KOSTAS, S. A., DRIVER, S. E., and MELLO, C. C. 1998. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 391:806–811.PubMedCrossRefGoogle Scholar
  27. FOTHERGILL, J. L., PANAGEA, S., HART, C. A., WALSHAW, M. J., PITT, T. L., and WINSTANLEY, C. 2007. Widespread pyocyanin over-production among isolates of a cystic fibrosis epidemic strain. BMC Microbiol. 7:45.PubMedCrossRefGoogle Scholar
  28. GIVSKOV, M., De NYS, R., MANEFIELD, M., GRAM, L., MAXIMILIEN, R., EBERL, L., MOLIN, S., STEINBERG, P. D., and KJELLEBERG, S. 1996. Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J. Bacteriol. 178:6618–6622.PubMedGoogle Scholar
  29. GOLDEN, J. W., and RIDDLE, D. L. 1982. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science. 218:578–580.PubMedCrossRefGoogle Scholar
  30. HEDBLOM, M. L., and ADLER, J. 1983. Chemotactic response of Escherichia coli to chemically synthesized amino acids. J. Bacteriol. 155:1463–1466.PubMedGoogle Scholar
  31. HUIXIN, L., INUBUSHI, K., and MIWA, J. 2001. Effects of temperature on population growth and n mineralization of soil bacteria and a bacterial-feeding nematode. Microb. Environ. 16:141–146.CrossRefGoogle Scholar
  32. JAFFE, H., HUETTEL, R. N., DEMILO, A. B., HAYS, D. K., and REBOIS, R. V. 1989. Isolation and identification of a compound from soybean cyst nematode, Heterodera glycines, with sex pheromone activity. J. Chem. Ecol. 15:2031–2043.CrossRefGoogle Scholar
  33. JEONG, P. Y., JUNG, M., YIM, Y. H., KIM, H., PARK, M., HONG, E., LEE, W., KIM, Y. H., KIM, K., and PAIK, Y. K. 2005. Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature. 433:541–545.PubMedCrossRefGoogle Scholar
  34. JOHNSON, B. A. 2004. Using NMRView to visualize and analyze the NMR spectra of macromolecules. Methods Mol. Biol. 278:313–352.PubMedGoogle Scholar
  35. JOHNSON, R. A., and WICHERN, D. W. 2001. Applied Multivariate Statistical Analysis. Prentice Hall.Google Scholar
  36. JOHNSTONE, I. L. 1999. Molecular Biology, pp. 201–225, in I. A. Hope (ed.). C. elegans A Practical Approach. Oxford University Press, New York.Google Scholar
  37. KAMILOVA, F., KRAVCHENKO, L. V., SHAPOSHNIKOV, A. I., AZAROVA, T., MAKAROVA, N., and LUGTENBERG, B. 2006. Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol. Plant Microbe Interact. 19:250–256.PubMedCrossRefGoogle Scholar
  38. KUMAR, R., BHATIA, R., KUKREJA, K., BEHL, R. K., DUDEJA, S. S., and NARULA, N. 2007. Establishment of Azotobacter on plant roots: chemotactic response, development and analysis of root exudates of cotton (Gossypium hirsutum L.) and wheat (Triticum aestivum L.). J. Basic Microbiol. 47:436–439.PubMedCrossRefGoogle Scholar
  39. LUGTENBERG, B. J., KRAVCHENKO, L. V., and SIMONS, M. 1999. Tomato seed and root exudate sugars: composition, utilization by Pseudomonas biocontrol strains and role in rhizosphere colonization. Environ. Microbiol. 1:439–446.PubMedCrossRefGoogle Scholar
  40. MARKLEY, J. L., ANDERSON, M. E., CUI, Q., EGHBALNIA, H. R., LEWIS, I. A., HEGEMAN, A. D., LI, J., SCHULTE, C. F., SUSSMAN, M. R., WESTLER, W. M., ULRICH, E. L., and ZOLNAI, Z. 2007. New bioinformatics resources for metabolomics. Pac. Symp. Biocomput.:157–168.Google Scholar
  41. MESIBOV, R., and ADLER, J. 1972. Chemotaxis toward amino acids in Escherichia coli. J. Bacteriol. 112:315–326.PubMedGoogle Scholar
  42. MILLER, M. B., and BASSLER, B. L. 2001. Quorum sensing in bacteria. Annu. Rev. Microbiol. 55:165–199.PubMedCrossRefGoogle Scholar
  43. MOLINA, L., RAMOS, C., DUQUE, E., RONCHEL, M. C., GARCIA, J. M., WYKE, L., and RAMOS, J. L. 2000. Survival of Pseudomonas putida KT2440 in soil and in the rhizosphere of plants under greenhouse and environmental conditions. Soil Biol. Biochem. 32:315–321.CrossRefGoogle Scholar
  44. MOULTON, R. C., and MONTIE, T. C. 1979. Chemotaxis by Pseudomonas aeruginosa. J. Bacteriol. 137:274–280.PubMedGoogle Scholar
  45. PARK, S., WOLANIN, P. M., YUZBASHYAN, E. A., LIN, H., DARNTON, N. C., STOCK, J. B., SILBERZAN, P., and AUSTIN, R. 2003. Influence of topology on bacterial social interaction. Proc. Natl. Acad. Sci. U. S. A. 100:13910–13915.PubMedCrossRefGoogle Scholar
  46. PEARSON, J. P., PESCI, E. C., and IGLEWSKI, B. H. 1997. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol. 179:5756–5767.PubMedGoogle Scholar
  47. PERSSON, T., HANSEN, T. H., RASMUSSEN, T. B., SKINDERSO, M. E., GIVSKOV, M., and NIELSEN, J. 2005. Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org. Biomol. Chem. 3:253–262.PubMedCrossRefGoogle Scholar
  48. PUNGALIYA, C., SRINIVASAN, J., FOX, B. W., MALIK, R. U., LUDEWIG, A. H., STERNBERG, P. W., and SCHROEDER, F. C. 2009. A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 106:7708–7713.PubMedCrossRefGoogle Scholar
  49. RAMOS-GONZÁLEZ, M. I., CAMPOS, M. J., and RAMOS, J. L. 2005. Analysis of Pseudomonas putida KT2440 gene expression in the maize rhizosphere: in vivo [corrected] expression technology capture and identification of root-activated promoters. J. Bacteriol. 187:4033–4041.PubMedCrossRefGoogle Scholar
  50. RASMUSSEN, T. B., and GIVSKOV, M. 2006. Quorum-sensing inhibitors as anti-pathogenic drugs. Int. J. Med. Microbiol. 296:149–161.PubMedCrossRefGoogle Scholar
  51. RASMUSSEN, T. B., BJARNSHOLT, T., SKINDERSOE, M. E., HENTZER, M., KRISTOFFERSEN, P., KOTE, M., NIELSEN, J., EBERL, L., and GIVSKOV, M. 2005a. Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J. Bacteriol. 187:1799–1814.PubMedCrossRefGoogle Scholar
  52. RASMUSSEN, T. B., SKINDERSOE, M. E., BJARNSHOLT, T., PHIPPS, R. K., CHRISTENSEN, K. B., JENSEN, P. O., ANDERSEN, J. B., KOCH, B., LARSEN, T. O., HENTZER, M., EBERL, L., HOIBY, N., and GIVSKOV, M. 2005b. Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology. 151:1325–1340.PubMedCrossRefGoogle Scholar
  53. ROBINETTE, S. L., ZHANG, F., BRÜSCHWEILER-LI, L., and BRÜSCHWEILER, R. 2008. Web Server Based Complex Mixture Analysis by NMR. Anal. Chem. 80:3606–3611.PubMedCrossRefGoogle Scholar
  54. ROESSNER, U., WAGNER, C., KOPKA, J., TRETHEWEY, R. N., and WILLMITZER, L. 2000. Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J. 23:131–142.PubMedCrossRefGoogle Scholar
  55. SEAVEY, B. R., FARR, E. A., WESTLER, W. M., and MARKLEY, J. L. 1991. A relational database for sequence-specific protein NMR data. J. Biomol. NMR. 1:217–236.PubMedCrossRefGoogle Scholar
  56. SHAKA, A. J., LEE, C. J., and PINES, A. 1988. Iterative schemes for bilinear operators; application to spin decoupling. J. Magn. Reson. 77:274–293.Google Scholar
  57. SHTONDA, B. B., and AVERY, L. 2006. Dietary choice behavior in Caenorhabditis elegans. J. Exp. Biol. 209:89–102.PubMedCrossRefGoogle Scholar
  58. SIMON, J. M., and STERNBERG, P. W. 2002. Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 99:1598–1603.PubMedCrossRefGoogle Scholar
  59. SINGH, T., and ARORA, D. K. 2001. Motility and chemotactic response of Pseudomonas fluorescens toward chemoattractants present in the exudate of Macrophomina phaseolina. Microbiol. Res. 156:343–351.PubMedCrossRefGoogle Scholar
  60. SNYDER, D. A., ZHANG, F., ROBINETTE, S. L., BRÜSCHWEILER-LI, L., and BRÜSCHWEILER, R. 2008. Non-negative matrix factorization of two-dimensional NMR spectra: Application to complex mixture analysis. J. Chem. Phys. 128:052313.PubMedCrossRefGoogle Scholar
  61. SRINIVASAN, J., KAPLAN, F., AJREDINI, R., ZACHARIAH, C., ALBORN, H. T., TEAL, P. E., MALIK, R. U., EDISON, A. S., STERNBERG, P. W., and SCHROEDER, F. C. 2008. A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature. 454:1115–1118.PubMedCrossRefGoogle Scholar
  62. STIERNAGLE, T. 1999. Maintenance of C. elegans, pp. 51–67, in I. A. Hope (ed.). C. elegans A Practical Approach. Oxford University Press, New York.Google Scholar
  63. STOVER, C. K., PHAM, X. Q., ERWIN, A. L., MIZOGUCHI, S. D., WARRENER, P., HICKEY, M. J., BRINKMAN, F. S., HUFNAGLE, W. O., KOWALIK, D. J., LAGROU, M., GARBER, R. L., GOLTRY, L., TOLENTINO, E., WESTBROCK-WADMAN, S., YUAN, Y., BRODY, L. L., COULTER, S. N., FOLGER, K. R., KAS, A., LARBIG, K., LIM, R., SMITH, K., SPENCER, D., WONG, G. K., WU, Z., PAULSEN, I. T., REIZER, J., SAIER, M. H., HANCOCK, R. E., LORY, S., and OLSON, M. V. 2000. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature. 406:959–964.PubMedCrossRefGoogle Scholar
  64. SULSTON, J. E., SCHIERENBERG, E., WHITE, J. G., and THOMSON, J. N. 1983. The Embryonic-Cell Lineage of the Nematode Caenorhabditis elegans. Dev. Biol. 100:64–119.PubMedCrossRefGoogle Scholar
  65. TRBOVIC, N., SMIRNOV, S., ZHANG, F., and BRÜSCHWEILER, R. 2004. Covariance NMR spectroscopy by singular value decomposition. J. Magn. Reson. 171:277–283.PubMedCrossRefGoogle Scholar
  66. TSO, W. W., and ADLER, J. 1974. Negative chemotaxis in Escherichia coli. J. Bacteriol. 118:560–576.PubMedGoogle Scholar
  67. Van Der DRIFT, C., DUIVERMAN, J., BEXKENS, H., and KRIJNEN, A. 1975. Chemotaxis of a motile Streptococcus toward sugars and amino acids. J. Bacteriol. 124:1142–1147.PubMedGoogle Scholar
  68. WAGNER, C., SEFKOW, M., and KOPKA, J. 2003. Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochemistry. 62:887–900.PubMedCrossRefGoogle Scholar
  69. WALKER, T. S., BAIS, H. P., DEZIEL, E., SCHWEIZER, H. P., RAHME, L. G., FALL, R., and VIVANCO, J. M. 2004. Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol. 134:320–331.PubMedCrossRefGoogle Scholar
  70. WHITE, J. G., SOUTHGATE, E., THOMSON, J. N., and BRENNER, S. 1986. The Structure of the Nervous-System of the Nematode Caenorhabditis elegans. Philos. Trans. R. Soc. B-Biol. Sci. 314:1–340.CrossRefGoogle Scholar
  71. WHITE, J. Q., NICHOLAS, T. J., GRITTON, J., TRUONG, L., DAVIDSON, E. R., and JORGENSEN, E. M. 2007. The sensory circuitry for sexual attraction in C. elegans males. Curr. Biol. 17:18471857.PubMedCrossRefGoogle Scholar
  72. WILLIAMS, P., WINZER, K., CHAN, W. C., and CAMARA, M. 2007. Look who’s talking: communication and quorum sensing in the bacterial world. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 362:1119–1134.PubMedCrossRefGoogle Scholar
  73. WILSON, R., AINSCOUGH, R., ANDERSON, K., BAYNES, C., BERKS, M., BURTON, J., CONNELL, M., BONFIELD, J., COPSEY, T., COOPER, J., COULSON, A., CRAXTON, M., DEAR, S., DU, Z., DURBIN, R., FAVELLO, A., FRASER, A., FULTON, L., GARDNER, A., GREEN, P., HAWKINS, T., HILLIER, L., JIER, M., JOHNSTON, L., JONES, M., KERSHAW, J., KIRSTEN, J., LAISSTER, N., LATREILLE, P., LLOYD, C., MORTIMORE, B., OCALLAGHAN, M., PARSONS, J., PERCY, C., RIFKEN, L., ROOPRA, A., SAUNDERS, D., SHOWNKEEN, R., SIMS, M., SMALDON, N., SMITH, A., SMITH, M., SONNHAMMER, E., STADEN, R., SULSTON, J., THIERRYMIEG, J., THOMAS, K., VAUDIN, M., VAUGHAN, K., WATERSTON, R., WATSON, A., WEINSTOCK, L., WILKINSONSPROAT, J., and WOHLDMAN, P. 1994. 2.2 Mb of Contiguous Nucleotide-Sequence from Chromosome-Iii of C. elegans. Nature. 368:32–38.PubMedCrossRefGoogle Scholar
  74. YU, H. S., and ALAM, M. 1997. An agarose-in-plug bridge method to study chemotaxis in the Archaeon Halobacterium salinarum. FEMS Microbiol. Lett. 156:265–269.PubMedCrossRefGoogle Scholar
  75. YUAN, J. Y., SHAHAM, S., LEDOUX, S., ELLIS, H. M., and HORVITZ, H. R. 1993. The C. elegans Cell-Death Gene Ced-3 Encodes a Protein Similar to Mammalian Interleukin-1-Beta-Converting Enzyme. Cell. 75:641–652.PubMedCrossRefGoogle Scholar
  76. ZAHRADNÍČKOVÁ, H., HUŠEK, P., ŠIMEK, P., HARTVICH, P., MARŠÁLEK, B., and HOLOUBEK, I. 2007. Determination of D- and L-amino acids produced by cyanobacteria using gas chromatography on Chirasil-Val after derivatization with pentafluoropropyl chloroformate. Anal. Bioanal. Chem. 388:1815–1822.PubMedCrossRefGoogle Scholar
  77. ZHANG, F., and BRÜSCHWEILER, R. 2007. Robust deconvolution of complex mixtures by covariance TOCSY spectroscopy. Angew. Chem. Int. Ed. 46:2639–2642.CrossRefGoogle Scholar
  78. ZHANG, F., DOSSEY, A. T., ZACHARIAH, C., EDISON, A. S., and BRÜSCHWEILER, R. 2007. Strategy for automated analysis of dynamic metabolic mixtures by NMR. Application to an insect venom. Anal. Chem. 79:7748–7752.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Fatma Kaplan
    • 1
  • Dayakar V. Badri
    • 2
  • Cherian Zachariah
    • 3
    • 4
    • 5
  • Ramadan Ajredini
    • 3
    • 4
    • 5
  • Francisco J. Sandoval
    • 6
  • Sanja Roje
    • 6
  • Lanfang H. Levine
    • 7
  • Fengli Zhang
    • 8
  • Steven L. Robinette
    • 3
    • 4
    • 5
  • Hans T. Alborn
    • 1
  • Wei Zhao
    • 9
  • Michael Stadler
    • 3
    • 4
    • 5
  • Rathika Nimalendran
    • 3
    • 4
    • 5
  • Aaron T. Dossey
    • 3
    • 4
    • 5
  • Rafael Brüschweiler
    • 8
  • Jorge M. Vivanco
    • 2
  • Arthur S. Edison
    • 3
    • 4
    • 5
  1. 1.Center for Medical, Agricultural and Veterinary EntomologyUSDA-ARSGainesvilleUSA
  2. 2.Center for Rhizosphere BiologyColorado State UniversityFort CollinsUSA
  3. 3.Department of Biochemistry & Molecular BiologyUniversity of FloridaGainesvilleUSA
  4. 4.National High Magnetic Field LaboratoryUniversity of FloridaGainesvilleUSA
  5. 5.McKnight Brain InstituteUniversity of FloridaGainesvilleUSA
  6. 6.Institute of Biological ChemistryWashington State UniversityPullmanUSA
  7. 7.Dynamac CorporationKennedy Space CenterBrevard CountyUSA
  8. 8.National High Magnetic Field Laboratory and Dept of ChemistryFlorida State UniversityTallahasseeUSA
  9. 9.St. Jude Children’s Research HospitalMemphisUSA

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