Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-18T10:42:48.108Z Has data issue: false hasContentIssue false

An investigation of chemotaxis in the insect parasitic nematode Heterorhabditis bacteriophora

Published online by Cambridge University Press:  17 October 2003

D. M. O'HALLORAN
Affiliation:
Institute of Bioengineering and Agroecology and Department of Biology, National University of Ireland Maynooth, Maynooth, Co.Kildare, Ireland
A. M. BURNELL
Affiliation:
Institute of Bioengineering and Agroecology and Department of Biology, National University of Ireland Maynooth, Maynooth, Co.Kildare, Ireland

Abstract

We tested the chemotactic responses of dauer juvenile stages (DJs) of the insect parasitic nematode Heterorhabditis bacteriophora to a variety of compounds that are known to be highly attractive or highly repellent to Caenorhabditis elegans. While H. bacteriophora DJs respond to alcohols and some aromatic compounds as well as to host metabolites such as uric acid and CO2, the most notable difference in the responses of these two nematodes is that H. bacteriophora DJs are unresponsive to a large number of compounds which C. elegans finds highly attractive. The latter compounds are typical by-products of bacterial metabolism and include aldehydes, esters, ketones and short-chain alcohols. While C. elegans finds long-chain alcohols (e.g. 1-heptanol and 1-octanol) repellent and short-chain alcohols highly attractive, H. bacteriophora DJs are strongly attracted to 1-heptanol, 1-octanol and 1-nonanol and find short-chain alcohols to be only slightly attractive. Parasitic-stage H. bacteriophora nematodes show a very weak chemotactic response to volatile molecules that DJs find highly attractive. Our results suggest that, associated with the adoption of a parasitic mode of life by Heterorhabditis, there was an adaptive change in chemotactic behaviour of the infective stages, resulting in a decreased sensitivity to volatile by-products of bacterial metabolism and an increased sensitivity towards long-chain alcohols and other insect-specific volatiles and possibly also to herbivore-induced plant volatiles.

Type
Research Article
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ANDREW, P. A. & NICHOLAS, W. L. (1976). Effect of bacteria on dispersal of Caenorhabditis elegans (Rhabditidae). Nematologica 221, 451461.CrossRefGoogle Scholar
ASHTON, F. T., LI, J. & SCHAD, G. A. (1999). Chemo- and thermosensory neurons: structure and function in animal parasitic nematodes. Veterinary Parasitology 84, 297316.CrossRefGoogle Scholar
BALAN, J. (1985). Measuring minimal concentrations of attractants detected by the nematode Panagrellus redivivus. Journal of Chemical Ecology 11, 105111.CrossRefGoogle Scholar
BALANOVA, J. & BALAN, J. (1991). Chemotaxis-controlled search for food by the nematode Panagrellus redivivus. Biologia 46, 257263.Google Scholar
BARGMANN, C. I., HARTWEIG, E. & HORVITZ, H. R. (1993). Odorant selective genes and neurons mediate olfaction in C. elegans. Cell 74, 515527.CrossRefGoogle Scholar
BARGMANN, C. I. & HORVITZ, H. R. (1991). Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7, 729742.CrossRefGoogle Scholar
BARGMANN, C. I. & MORI, I. (1997). Chemotaxis and thermotaxis. In C. elegans II (ed. Riddle, D. L., Blumenthal, T., Meyer, B. J. & Preiss, J. R.), pp. 717738. Cold Spring Harbor Press, New York.
BATE, N. J., RILEY, J. C. M., THOMPSON, J. E. & ROTHSTEIN, S. J. (1998). Quantitative and qualitative differences in C-6-volatile production from the lipoxygenase pathway in an alcohol dehydrogenase mutant of Arabidopsis thaliana. Physiologia Plantarum 104, 97104.CrossRefGoogle Scholar
BLAXTER, M. L., DE LEY, P., GAREY, J. R., LIU, L. X., SCHELDEMAN, P., VIERSTRAETE, A., VANFLETEREN, J. R., MACKEY, L. Y., DORRIS, M., FRISSE, L. M., VIDA, J. T. & THOMAS, W. K. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature, London 392, 7175.CrossRefGoogle Scholar
BOEMARE, N. E., AKHURST, R. J. & MOURANT, R. G. (1993). DNA relatedness between Xenorhabdus spp. (Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes, and a proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen-nov. International Journal of Systematic Bacteriology 43, 249255.Google Scholar
BRENNER, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 7194.Google Scholar
BUCK, L. & AXEL, R. (1991). A novel multigene family may encode odorant receptors – a molecular-basis for odor recognition. Cell 65, 175187.CrossRefGoogle Scholar
CASSADA, R. C. & RUSSELL, R. L. (1975). The dauer larva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Developmental Biology 46, 326342.CrossRefGoogle Scholar
CLYNE, P. J., WARR, C. G., FREEMAN, M. R., LESSING, D., KIM, J. H. & CARLSON, J. R. (1999). A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22, 327338.CrossRefGoogle Scholar
CONSOULAS, C., DUCH, C., BAYLINE, R. J. & LEVINE, R. B. (2000). Behavioral transformations during metamorphosis: remodeling of neural and motor systems. Brain Research Bulletin 53, 571583.CrossRefGoogle Scholar
CULOTTI, L. G. & RUSSELL, R. L. (1978). Osmotic avoidance defective mutants of the nematode Caenorhabditis elegans. Genetics 90, 243256.Google Scholar
DICKE, M. (1999). Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomologia Experimentalis et Applicata 91, 131142.Google Scholar
DOLAN, K. M., JONES, J. T. & BURNELL, A. M. (2002). Detection of changes occurring during recovery from the dauer stage in Heterorhabditis bacteriophora. Parasitology 125, 7181.CrossRefGoogle Scholar
DUBIN, A. E., HEALD, N. L., CLEVELAND, B., CARLSON, J. R. & HARRIS, G. L. (1995). Scutoid mutation of Drosophila melanogaster specifically decreases olfactory responses to short-chain acetate esters and ketones. Journal of Neurobiology 28, 214233.CrossRefGoogle Scholar
DUSENBERY, D. B. (1974). Analysis of chemotaxis in the nematode Caenorhabditis elegans by countercurrent separation. Journal of Experimental Zoology 188, 4147.CrossRefGoogle Scholar
FORST, S., DOWDS, B., BOEMARE, N. & STACKEBRANDT, E. (1997). Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annual Review of Microbiology 51, 4772.Google Scholar
GAUGLER, R., LEBECK, L., NAGAKI, B. & BOUSH, G. M. (1980). Orientation of the entomogenous nematode Neoaplectana carpocapsae to carbon dioxide. Environmental Entomology 9, 649652.CrossRefGoogle Scholar
GEERVLIET, J. B. F., POSTHUMUS, M. A., VET, L. E. M. & DICKE, M. (1997). Comparative analysis of headspace volatiles from different caterpillar-infested or uninfested food plants of Pieris species. Journal of Chemical Ecology 23, 29352954.CrossRefGoogle Scholar
GOLDEN, J. W. & RIDDLE, D. L. (1984). The Caenorhabditis elegans dauer larva: developmental effects of pheromone, food, and temperature. Developmental Biology 102, 368378.CrossRefGoogle Scholar
GRANT, W. N. & VINEY, M. E. (2001). Post-genomic nematode parasitology. International Journal for Parasitology 31, 879888.CrossRefGoogle Scholar
GREWAL, P. S., GAUGLER, R. & LEWIS, E. E. (1993). Host recognition behavior by entomopathogenic nematodes during contact with insect gut contents. Journal of Parasitology 79, 495503.CrossRefGoogle Scholar
HAN, B. Y. & CHEN, Z. M. (2002). Composition of the volatiles from intact and mechanically pierced tea aphid-tea shoot complexes and their attraction to natural enemies of the tea aphid. Journal of Agricultural and Food Chemistry 50, 25712575.CrossRefGoogle Scholar
HEBETS, E. A. & CHAPMAN, R. F. (2000). Electrophysiological studies of olfaction in the whip spider Phrynus parvulus (Arachnida, Amblypygi). Journal of Insect Physiology 46, 14411448.CrossRefGoogle Scholar
KHLIBSUWAN, W., ISHIBASHI, N. & KONDO, E. (1992). Response of Steinernema carpocapsae infective juveniles to the plasma of three insect species. Journal of Nematology 24, 156159.Google Scholar
KRIEGER, J. & BREER, H. (1999). Olfactory reception in invertebrates. Science 286, 720723.CrossRefGoogle Scholar
LEWIS, E. E. (2002). Behavioural Ecology. In Entomopathogenic Nematology (ed. Gaugler, R.), pp. 205223. CABI Publishing, Wallingford, Oxon, UK.CrossRef
LEWIS, E. E., GAUGLER, R. & HARRISON, R. (1992). Entomopathogenic nematode host finding: response to host contact cues by cruise and ambush foragers. Parasitology 105, 309315.CrossRefGoogle Scholar
LEWIS, E. E., GLAZER, I. & GAUGLER, R. (1996). Location and behavioral effects of lectin binding on entomopathogenic nematodes with different foraging strategies. Journal of Chemical Ecology 22, 455466.CrossRefGoogle Scholar
MEINERS, T., WACKERS, F. & LEWIS, W. J. (2002). The effect of molecular structure on olfactory discrimination by the parasitoid Microplitis croceipes. Chemical Senses 27, 811816.CrossRefGoogle Scholar
O'LEARY, S. A., STACK, C. M., CHUBB, M. A. & BURNELL, A. M. (1998). The effect of day of emergence from the insect cadaver on the behaviour and environmental tolerances of infective juveniles of the entomopathogenic nematode Heterorhabditis megidis (Strain UK211). Journal of Parasitology 84, 665672.CrossRefGoogle Scholar
PRASAD, B. C. & REED, R. R. (1999). Chemosensation – molecular mechanisms in worms and mammals. Trends in Genetics 15, 150153.CrossRefGoogle Scholar
ROBINSON, A. F. (1995). Optimal release rates for attracting Meloidogyne incognita, Rotylenchulus reinformis, and other nematodes to carbon dioxide in sand. Journal of Nematology 27, 4250.Google Scholar
SANT'ANA, J. & DICKENS, J. C. (1998). Comparative electrophysiological studies of olfaction in predaceous bugs, Podisus maculiventris and P. nigrispinus. Journal of Chemical Ecology 24, 965984.CrossRefGoogle Scholar
SCHMIDT, J. & ALL, J. N. (1978). Attraction of Neoaplectana carpocapsae (Nematoda: Steinernematidae) to common excretory products of insects. Environmental Entomology 7, 605607.CrossRefGoogle Scholar
SCHÖLLER, C., MOLIN, S. & WILKINS, K. (1997). Volatile metabolites from some gram-negative bacteria. Chemosphere 35, 14871495.CrossRefGoogle Scholar
SCIACCA, J., FORBES, W. M., ASHTON, F. T., LOMBARDINI, E., GAMBLE, H. R. & SCHAD, G. A. (2002). Response to carbon dioxide by the infective larvae of three species of parasitic nematodes. Parasitology International 51, 5362.CrossRefGoogle Scholar
SENGUPTA, P., CHOU, J. H. & BARGMANN, C. I. (1996). odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84, 899909.CrossRefGoogle Scholar
SHAVER, S. A., VARNAM, C. J., HILLIKER, A. J., SOKOLOWSKI, M. B. (1998). The foraging gene affects adult but not larval olfactory-related behavior in Drosophila melanogaster. Behavioural Brain Research 95, 2329.CrossRefGoogle Scholar
SUDHAUS, W. (1993). Die mittels symbiontischer Bakterien entomopathogenen Nematoden Gattungen Heterorhabditis and Steinernema sind keine Schwestertaxa. Verhandlungen der Deutschen Zoologischen Gesellschaft 86, 146.Google Scholar
TROEMEL, E. R., CHOU, J. H., DWYER, N. D., COLBERT, H. A. & BARGMANN, C. I. (1995). Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elgans. Cell 83, 207218.CrossRefGoogle Scholar
VAN TOL, R. W. H. M., VAN DER SOMMEN, A. T. C., BOFF, M. I. C., VAN BEZOOIJEN, J., SABELIS, M. W. & SMITS, P. H. (2001). Plants protect their roots by alerting the enemies of grubs. Ecology Letters 4, 292294.Google Scholar
VOSSHALL, L. B., AMREIN, H., MOROZOV, P. S., RZHETSKY, A. & AXEL, R. (1999). A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96, 725736.CrossRefGoogle Scholar
WARD, S. (1973). Chemotaxis by the nematode Caenorhabditis elegans: identification of attractants and analysis of the response by use of mutants. Proceedings of the National Academy of Sciences, USA 70, 817821.CrossRefGoogle Scholar
WHITE, G. F. (1927). A method for obtaining infective larvae from cultures. Science 66, 302303.CrossRefGoogle Scholar
WOODRING, J. L. & KAYA, H. K. (1988). Steinernematid and heterorhabditid nematodes: a handbook of biology and techniques. Southern Cooperative Series Bulletin No. 331, Arkansas Agricultural Experiment Station, Fayetteville, Arkansas.
ZECHMAN, J. M. & LABOWS, J. N. J. (1985). Volatiles of Pseudomonas aeruginosa and related species by automated headspace concentration gas chromatography. Canadian Journal of Micobiology 31, 232237.CrossRefGoogle Scholar