Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T19:03:14.588Z Has data issue: false hasContentIssue false

Adhesion of Pasteuria penetrans to the cuticle of root-knot nematodes (Meloidogyne spp.) inhibited by fibronectin: a study of electrostatic and hydrophobic interactions

Published online by Cambridge University Press:  06 April 2009

K. G. Davies
Affiliation:
Entomology and Nematology Department, AFRC-Institute of Arable Crops Research, Rothamsted Experimental Station, Harpenden, Hertfordshire AL5 2JQ
P. Afolabi
Affiliation:
Department of Biological and Chemical Sciences, University of Essex, Wivenhoe Park, Colchester, Essex CO4 3SQ
P. O'Shea*
Affiliation:
Department of Biological and Chemical Sciences, University of Essex, Wivenhoe Park, Colchester, Essex CO4 3SQ
*
* Corresponding author. Fax: + 44 1206 872592. E-mail: [email protected].

Summary

Pasteuria penetrans is a bacterium with the potential to control plant-parasitic nematode populations; the mechanism of spore adhesion, however, is poorly understood. Attachment assays were performed in media supplemented with various concentrations of fibronectin and in the presence and absence of KSCN which modulates hydrophobic interactions. A reduction in the strength of the hydrophobic effect prevented spores from binding to the cuticle as did 20 μg/ml fibronectin. It was also shown directly utilizing a newly-developed technique which utilizes 3-hexadecanoyl-7-hydro-coumarin as an indicator of the fibronectin binding to the spore surface that the presence of KSCN prohibited binding. This effect was interpreted to indicate that the reduction of binding was the direct result of the influence of hydrophobic interactions between the fibronectin and the spore surface. Western blot analysis of cuticle extracts of Meloidogyne incognita and Caenorhabditis elegans revealed small amounts of fibronectin to be present. Fibronectin, or a similar receptor, present in the cuticle could be responsible for the adhesion of P. penetrans by hydrophobic interactions.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1996

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

Afolabi, P., Davies, K. G. & O'Shea, P. (1995). The electrostatic nature of the spore of Pasteuria penetrans, the bacterial parasite of root-knot nematodes. Journal of Applied Bacteriology 79, 244–9.CrossRefGoogle Scholar
Benian, G. M., Kiff, J. E., Neckelmann, N., Moerman, D. G. & Waterstone, R. H. (1989). Sequence of an unusually large protein implicated in the regulation of myosin activity in C. elegans. Nature, London 342, 4550.CrossRefGoogle ScholarPubMed
Benian, G. M., L'Hernault, S. W. & Morris, M. E. (1993). Additional sequence complexity in the muscle gene, unc-22, and its encoded protein, twitchin, of Caenorhabditis elegans. Genetics 134, 1097–104.CrossRefGoogle ScholarPubMed
Blaxter, M. L., Page, A. P., Rudin, W. & Maizels, R. M. (1992). Nematode surface coats: actively evading immunity. Parasitology Today 8, 243–6.CrossRefGoogle ScholarPubMed
Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 7194.CrossRefGoogle ScholarPubMed
Carson, S. E. (1989). The structure and function of fibronectins. In Fibronectin in Health and Disease (ed. Carsons, S. E.) pp. 121. CRC Press, Boca Raton, Florida.Google Scholar
Channer, A. G. De R. & Gowen, S. R. (1992). Selection for increased host resistance and increased pathogen specificity in the Meloidogyne-Pasteuria penetrans interaction. Fundamental and Applied Nematology 15, 331–9.Google Scholar
Courtney, H. S., Hasty, D. L. & Ofek, I. (1990). Hydrophobicity of group A streptococci and its relationship to adhesion of streptoccoci to host cells. In Microbial Cell Hydrophobicity, (ed. Doyle, R. J. & Rosenberg, M.), pp. 361386. American Society for Microbiology, Washington.Google Scholar
Davies, K. G. (1994). A nematode case study focusing on the application of serology. In Identification and Characterisation of Pest Organisms (ed. Hawksworth, D. L.), pp. 395413. CAB International, Wallingford.Google Scholar
Davies, K. G. & Danks, c. (1992). Interspecific differences in the nematode surface coat between Meloidogyne incognita and M. arenaria related to the adhesion of the bacterium Pasteuria penetrans. Parasitology 105, 475–80.CrossRefGoogle Scholar
Davies, K. G. & Danks, C. (1993). Carbohydrate/protein interactions between the cuticle of infective juveniles of Meloidogyne incognita and spores of the obligate hyperparasite Pasteuria penetrans. Nematologica 39, 5364.Google Scholar
Davies, K. G. & Lander, E. B. (1992). Immunological differentiation of root-knot nematodes (Meloidogyne spp.) using monoclonal and polyclonal antibodies. Nematologica 38, 353–66.CrossRefGoogle Scholar
Davies, K. G., Pearson, T. & Redden, M. (1994). Endospore heterogeneity in Pasteuria penetrans related to adhesion to plant parasitic nematodes. Letters in Applied Microbiology 19, 370–3.CrossRefGoogle Scholar
Georgis, R. & Mannweiler, S. A. (1994). Entomopathogenic nematodes: A developing biological control technology. Agricultural Zoology Reviews 6, 6394.Google Scholar
Grant, W. N. (1992). Transformation of Caenorhabditis elegans with genes from parasitic nematodes. Parasitology Today 8, 344–6.CrossRefGoogle ScholarPubMed
Harlow, E. & Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbour.Google Scholar
Hasty, D. L., Beachey, E. H., Courtney, H. S. & Simpson, W. A. (1989). Interactions between fibronectin and bacteria. In Fibronectin in Health and Disease (ed. Carsons, S. E.), pp. 89112. Boca Raton, Florida: CRC Press.Google Scholar
Hatefi, Y. & Hanstein, W. G. (1969). Solubilization of particulate proteins and non-electrolytes by chaotropic agents. Proceedings of the National Academy Sciences, USA 62, 1129–36.CrossRefGoogle Scholar
Hemmer, R. M., Donkin, S. G., Chin, K. J., Grenache, D. G., Bhatt, H. & Politz, S. M. (1991). Altered expression of an L1-specific, O-linked cuticle surface glycoprotein in mutants of the nematode Caenorhabditis elegans. Journal of Cell Biology 115, 1237–47.CrossRefGoogle ScholarPubMed
Hewlett, T. E. & Dickson, D. W. (1993). A centrifugation method for attaching endospores of Pasteuria spp. to nematodes. Supplement to Journal of Nematology 25, 785–8.Google ScholarPubMed
Hooper, D. J. (1986). Extraction of nematodes from plant material. In Laboratory Methods for Work with Plants and Soil Nematodes. (ed. Southey, J. F.), pp. 5158. Ministry of Agriculture Fisheries and Food, London, HMSO.Google Scholar
Kramer, J. M. (1994). Genetic analysis of extracellular matrix in C. elegans. Annual Review of Genetics 28, 95116.CrossRefGoogle ScholarPubMed
Moerman, D. G., Benian, G. M., Barsted, D. R. J., Schriefer, L. A. & Waterstone, R. H. (1988). Identification and intracellular localisation of the unc-22 gene product of Caenorhabditis elegans. Genes and Development 2, 93105.CrossRefGoogle ScholarPubMed
Oostendorp, M., Dickson, D. W. & Mitchell, D. J. (1991). Population development of Pasteuria penetrans on Meloidogyne arenaria. Journal of Nematology 23, 5864.Google ScholarPubMed
Patti, J. M., Allen, B. L., McGavin, M. J. & Höök, M. (1994). MSCRAMM-Mediated adherence of microorganisms to host tissues. Annual Review Microbiology 48, 585617.CrossRefGoogle ScholarPubMed
Persidis, A., Lay, J. G., Manousis, T., Bishop, A. H. & Ellar, D. J. (1992). Characterisation of potential adhesins of the bacterium Pasteuria penetrans, and of putative receptors on the cuticle of Meloidogyne incognita, a nematode host. Journal of Cell Science 100, 613–22.Google Scholar
Politz, S. M. & Philipp, M. (1992). Caenorhabditis elegans as a model for parasitic nematodes: A focus on the cuticle. Parasitology Today 8, 612.CrossRefGoogle Scholar
Reddigari, S. R., Jansma, P. L., Premachandran, D. & Hussey, R. S. (1986). Cuticular collagenous proteins of second-stage juveniles and adult females of Meloidogyne incognita: isolation and partial characterisation. Journal of Nematology 18, 294302.Google Scholar
Sayre, R. M. & Starr, M. P. (1988). Bacterial diseases and antagonisms of nematodes. In Diseases of Nematodes, Vol. 1, (ed. Poinar, G. O. & Jansson, H. B. Jr.), pp. 69101. Boca Raton, Florida: CRC Press.Google Scholar
Sayre, R. M. & Starr, M. P. (1989). Genus Pasteuria Metchnikoff 1888, 166, emend. Sayre and Starr 1985, 149, Starr and Sayre 1988a, 27 (Nom. Cons. Opin. 61 Jud. Comm. 1986, 119. Not Pasteuria in the sence of Henrici and Johnson (1935), Hirsch (1972), or Staley (1973); see Starr et al. (1983) and Judicial Commission (1986)). In Bergey's Manuel of Systematic Bacteriology, Vol 4. (ed. Williams, S. T., Sharpe, M. E. & Holt, J. G.), pp. 26012621. London: Williams & Wilkins.Google Scholar
Sasser, J. N. & Freckman, D. W. (1987). A world perspective on nematology: The role of the society. In Vistas of Nematology (ed. Veech, J. A. & Dickson, D. W.), pp. 714. Society of Nematologists, Inc., Hyattsville, Maryland.Google Scholar
Stirling, G. R. (1991). Biological Control of Plant-Parasitic Nematodes: Progress, Problems and Prospects. CABI: Wallingford.Google Scholar
Stirling, G. R. & Wachtel, M. F. (1980). Mass production of Bacillus penetrans for the biological control of root-knot nematodes. Nematologica 26, 308–12.CrossRefGoogle Scholar
Thomason, I. J. (1987). Challenges facing nematology: environmental risks with nematicides and the need for new approaches. In Vistas of Nematology (ed. Veech, J. A. & Dickson, D. W.), pp. 469476. Society of Nematologists, Inc., Hyattsville, Maryland.Google Scholar
Wall, J., Ayoub, F. & O'Shea, p. (1995). The interactions of macromolecules with the mammalian cell surface. Journal of Cell Science 108, 2673–82.CrossRefGoogle ScholarPubMed