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Natural variation in the response of Caenorhabditis elegans towards Bacillus thuringiensis

Published online by Cambridge University Press:  16 April 2004

H. SCHULENBURG
Affiliation:
Department of Evolutionary Biology, Institute for Animal Evolution and Ecology, Westphalian Wilhelms-University, Hüfferstrasse 1, 48149 Münster, Germany
S. MÜLLER
Affiliation:
Department of Evolutionary Biology, Institute for Animal Evolution and Ecology, Westphalian Wilhelms-University, Hüfferstrasse 1, 48149 Münster, Germany

Abstract

Almost nothing is known about the natural ecology of the nematode Caenorhabditis elegans, including its interactions with parasites. To help rectify this discrepancy, we assessed natural variation in the response of C. elegans towards a potential parasite, the soil bacterium Bacillus thuringiensis. Our results show that 10 isolates from across the world differ significantly in survival rate and infection level when confronted with a parasitic strain of B. thuringiensis. Furthermore, behavioural responses are identified as an important component of C. elegans defence, including evasion and possibly reduced ingestion of parasites. Again, the natural isolates show significant differences in these traits. In conclusion, worm defence is indicated to be complex and variable across space, implying that parasites play an important role in the ecology of this species. Based on these results, we expect C. elegans to be a promising model host for future analysis of the evolutionary dynamics of parasite–host interactions.

Type
Research Article
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

ABALLAY, A. & AUSUBEL, F. M. (2001). Programmed cell death mediated by ced-3 and ced-4 protects Caenorhabditis elegans from Salmonella typhimurium-mediated killing. Proceedings of the National Academy of Sciences, USA 98, 27352739.CrossRefGoogle Scholar
AGRAWAL, A. F. & LIVELY, C. M. (2001). Parasites and the evolution of self-fertilization. Evolution 55, 869879.CrossRefGoogle Scholar
ANDREW, P. A. & NICHOLAS, W. L. (1976). Effect of bacteria on dispersal of Caenorhabditis elegans (Rhabditidae). Nematologica 22, 451461.CrossRefGoogle Scholar
BARGMANN, C. I. & MORI, I. (1997). Chemotaxis and thermotaxis. In C. elegans II (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Priess, J. R. ), pp. 717737. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
BORGONIE, G., CLAEYS, M., LEYNS, F., ARNAUT, G., DE WAELE, D. & COOMANS, A. (1996). Effect of nematicidal Bacillus thuringiensis strains on free-living nematodes. 1. Light microscopic observations, species and biological stage specificity and identification of resistant mutants of Caenorhabditis elegans. Fundamental and Applied Nematology 19, 391398.Google Scholar
BORGONIE, G., VAN DRIESSCHE, R., LEYNS, F., ARNAUT, G., DE WAELE, D. & COOMANS, A. (1995). Germination of Bacillus thuringiensis spores in bacteriophagous nematodes (Nematoda: Rhabditida). Journal of Invertebrate Pathology 65, 6167.CrossRefGoogle Scholar
DARBY, C., COSMA, C. L., THOMAS, J. H. & MANOIL, C. (1999). Lethal paralysis of Caenorhabditis elegans by Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences, USA 96, 1520215207.CrossRefGoogle Scholar
DE BONO, M. & BARGMANN, C. I. (1998). Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94, 679689.CrossRefGoogle Scholar
DE BONO, M., TOBIN, D. M., DAVIS, M. W., AVERY, L. & BARGMANN, C. I. (2002). Social feeding in Caenorhabditis elegans is induced by neurons that detect averse stimuli. Nature, London 419, 899903.CrossRefGoogle Scholar
EWBANK, J. J. (2002). Tackling both sides of the host–pathogen equation with Caenorhabditis elegans. Microbes and Infection 4, 247256.CrossRefGoogle Scholar
FRANK, S. A. (1996). Models of parasite virulence. Quarterly Review of Biology 71, 3778.CrossRefGoogle Scholar
GRIFFITHS, J. S., WHITACRE, J. L., STEVENS, D. E. & AROIAN, R. V. (2001). Bt toxin resistance from loss of a putative carbohydrate-modifying enzyme. Science 293, 860864.CrossRefGoogle Scholar
HAMILTON, W. D., AXELROD, R. & TANESE, R. (1990). Sexual reproduction as an adaptation to resist parasites: a review. Proceedings of the National Academy of Sciences, USA 87, 35663573.CrossRefGoogle Scholar
HODGKIN, J. & DONIACH, T. (1997). Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146, 149164.Google Scholar
HOPE, I. A. (1999). C. elegans: a Practical Approach. Oxford University Press, Oxford.
JOVELIN, R., AJIE, B. C. & PHILLIPS, P. C. (2003). Molecular evolution and quantitative variation for chemosensory behaviour in the nematode genus Caenorhabditis. Molecular Ecology 12, 13251337.CrossRefGoogle Scholar
KATO, Y., AIZAWA, T., HOSHINO, H., KAWANO, K., NITTA, K. & ZHANG, H. (2002). abf-1 and abf-2, ASABF-type antimicrobial peptide genes in Caenorhabditis elegans. Biochemical Journal 361, 221230.CrossRefGoogle Scholar
KIM, D. H., FEINBAUM, R., ALLOING, G., EMERSON, F. E., GARSIN, D. A., INOUE, H., TANAKA-HINO, M., HISAMOTO, N., MATSUMOTO, K., TAN, M. W. & AUSUBEL, F. M. (2002). A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297, 623626.CrossRefGoogle Scholar
KOCH, R., VAN LUENEN, H. G., VAN DER HORST, M., THIJSSEN, K. L. & PLASTERK, R. H. (2000). Single nucleotide polymorphisms in wild isolates of Caenorhabditis elegans. Genome Research 10, 16901696.CrossRefGoogle Scholar
KURZ, C. L. & EWBANK, J. J. (2003). Caenorhabditis elegans: an emerging genetic model for the study of innate immunity. Nature Reviews Genetics 4, 380390.CrossRefGoogle Scholar
LEYNS, F., BORGONIE, G., ARNAUT, G. & DE WAELE, D. (1995). Nematicidal activity of Bacillus thuringiensis isolates. Fundamental and Applied Nematology 18, 211218.Google Scholar
MAHAJAN-MIKLOS, S., TAN, M. W., RAHME, L. G. & AUSUBEL, F. M. (1999). Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96, 4756.CrossRefGoogle Scholar
MALLO, G., KURZ, C., COUILLAULT, C., PUJOL, N., GRANJEAUD, S., KOHARA, Y. & EWBANK, J. J. (2002). Inducible antibacterial defense system in C. elegans. Current Biology 12, 12091214.CrossRefGoogle Scholar
MARROQUIN, L. D., ELYASSNIA, D., GRIFFITTS, J. S., FEITELSON, J. S. & AROIAN, R. V. (2000). Bacillus thuringiensis (Bt) toxin susceptibility and isolation of resistance mutants in the nematode Caenorhabditis elegans. Genetics 155, 16931699.Google Scholar
O'QUINN, A. L., WIEGAND, E. M. & JEDDELOH, J. A. (2001). Burkholderia pseudomallei kills the nematode Caenorhabditis elegans using an endotoxin-mediated paralysis. Cell Microbiology 3, 381393.CrossRefGoogle Scholar
PARTRIDGE, L. & GEMS, D. (2002). Mechanisms of ageing: public or private? Nature Reviews Genetics 3, 165175.Google Scholar
PUJOL, N., LINK, E. M., LIU, L. X., KURZ, C. L., ALLOING, G., TAN, M. W., RAY, K. P., SOLARI, R., JOHNSON, C. D. & EWBANK, J. J. (2001). A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Current Biology 11, 809821.CrossRefGoogle Scholar
QUINN, G. P. & KEOUGH, M. J. (2002). Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.CrossRef
RIDDLE, D. L., BLUMENTHAL, T., MEYER, B. J. & PRIESS, J. R. (1997). C. elegans II. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
SIVASUNDAR, A. & HEY, J. (2003). Population genetics of Caenorhabditis elegans: the paradox of low polymorphism in a widespread species. Genetics 163, 147157.Google Scholar
SMITH, M. P., LAWS, T. R., ATKINS, T. P., OYSTON, P. C., DE POMERAI, D. I. & TITBALL, R. W. (2002). A liquid-based method for the assessment of bacterial pathogenicity using the nematode Caenorhabditis elegans. FEMS Microbiology Letters 210, 181185.CrossRefGoogle Scholar
SOKAL, R. R. & ROHLF, F. J. (1995). Biometry, 3 Edn. W.H. Freeman and Co., New York, USA.
STIERNAGLE, T. (1999). Maintenance of C. elegans. In C. elegans: a Practical Approach (ed. Hope, I. A. ), pp. 5167. Oxford University Press, Oxford.
WEI, J. Z., HALE, K., CARTA, L., PLATZER, E., WONG, C., FANG, S. C. & AROIAN, R. V. (2003). Bacillus thuringiensis crystal proteins that target nematodes. Proceedings of the National Academy of Sciences, USA 100, 27602765.CrossRefGoogle Scholar
WOOD, W. B. (1988). The Nematode Caenorhabditis elegans. Cold Springer Harbor Laboratory Press, Cold Spring Harbor.