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Cold tolerance in sealworm (Pseudoterranova decipiens) due to heat-shock adaptations

Published online by Cambridge University Press:  23 July 2009

S. K. STORMO ,
K. PRÆBEL  and
E. O. ELVEVOLL
S. K. STORMO*
Affiliation:
Department of Marine Biotechnology, University of Tromsø, N-9037 Tromsø, Norway
K. PRÆBEL
Affiliation:
Department of Aquatic BioSciences, Norwegian College of Fishery Science, University of Tromsø, N-9037 Tromsø, Norway
E. O. ELVEVOLL
Affiliation:
Department of Marine Biotechnology, University of Tromsø, N-9037 Tromsø, Norway
*
*Corresponding author: Tel: +47 77646722. Fax: +47 77646020. E-mail: [email protected].
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Summary

Third-stage larvae of Pseudoterranova decipiens commonly infect whitefish such as cod, and the parasite can be transferred to humans through lightly prepared (sushi) meals. Because little is known about the nematode's cold tolerance capacity, we examined the nematode's ability to supercool, and whether or not cold acclimation could induce physiological changes that might increase its ability to tolerate freezing conditions. Even if third-stage Pseudoterranova decipiens larvae have some supercooling ability, they show no potential for freezing avoidance because they are not able to withstand inoculative freezing. Still, they have the ability to survive freezing at high subzero temperatures, something which suggests that these nematodes have a moderate freeze tolerance. We also show that acclimation to high temperatures triggers trehalose accumulation to an even greater extent than cold acclimation. Trehalose is a potential cryoprotectant which has been shown to play a vital role in the freeze tolerance of nematodes. We suggest that the trehalose accumulation observed for the cold acclimation is a general response to thermal stress, and that the nematode's moderate freeze tolerance may be acquired through adaptation to heat rather than coldness.

Keywords

cold acclimationheat-shocktrehalose accumulationAnisakis simplexsupercooling point
Type
Research Article
Information
Parasitology , Volume 136 , Issue 11 , September 2009 , pp. 1317 - 1324
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Adams, A. M., Murrell, K. D. and Cross, J. H. (1997). Parasites of fish and risks to public health. Revue Scientifique Et Technique De L Office International Des Epizooties 16, 652–660.CrossRefGoogle ScholarPubMed
Arnarson, H., Bengoetxea, K. and Pau, L. F. (1991). Vision applications in the fishing and fish products industries. In Fish Quality Control by Computer Vision (ed. Pau, L. F. and Olafsson, R.), pp. 21–42. Marcel Dekker, New York, USA.Google Scholar
Audet, C., Besner, M., Munro, J. and Dutil, J. D. (1993). Seasonal and diel variations of various blood parameters in Atlantic cod (Gadus morhua) and American plaice (Hippoglossoides platessoides). Canadian Journal of Zoology-Revue Canadienne De Zoologie 71, 611–618.CrossRefGoogle Scholar
Audicana, M. T., Ansotegui, I. J., De Corres, L. F. and Kennedy, M. W. (2002). Anisakis simplex: dangerous – dead and alive? Trends in Parasitology 18, 20–25.CrossRefGoogle ScholarPubMed
Audicana, M. T., Del Pozo, M. D., Iglesias, R. and Ubeira, F. M. (2003). Anisakis simplex and Pseudoterranova decipiens. In International Handbook of Foodborne Pathogens (ed. Milliotis, M. D. and Bier, J. W.), pp. 613–636. Marcel Dekker, New York, USA.Google Scholar
Behm, C. A. (1997). The role of trehalose in the physiology of nematodes. International Journal for Parasitology 27, 215–229.CrossRefGoogle ScholarPubMed
Bublitz, C. G. and Choudhury, G. S. (1992). Effect of light intensity and color on worker productivity and parasite detection efficiency. Journal of Aquatic Food Product Technology 1, 75–88.CrossRefGoogle Scholar
Butt, A. A., Aldridge, K. E. and Sanders, C. V. (2004). Infections related to the ingestion of seafood. Part II: parasitic infections and food safety. Lancet Infectious Diseases 4, 294–300.CrossRefGoogle Scholar
Chen, S. L. and Chen, C. L. (1999). Effect of nucleation agents on the freezing probability of supercooled water inside capsules. Hvac&R Research 5, 339–351.CrossRefGoogle Scholar
Chen, S. L. and Lee, T. S. (1998). A study of supercooling phenomenon and freezing probability of water inside horizontal cylinders. International Journal of Heat and Mass Transfer 41, 769–783.CrossRefGoogle Scholar
Crowe, J. H., Hoekstra, F. A. and Crowe, L. M. (1992). Anhydrobiosis. Annual Review of Physiololy 54, 579–599.CrossRefGoogle ScholarPubMed
Davey, K. G., Sommerville, R. I. and Fuse, M. (1993). Stress-induced failure of osmoregulation in the parasitic nematode Pseudoterranova decipiens – indirect evidence for hormonal-regulation. Journal of Experimental Biology 180, 263–271.CrossRefGoogle ScholarPubMed
Davey, K. G. (1995). Water, water compartments and water regulation in some nematodes parasitic in vertebrates. Journal of Nematology 27, 433–440.Google ScholarPubMed
Deardorff, T. L. and Throm, R. (1988). Commercial blast-freezing of 3rd-stage Anisakis simplex larvae encapsulated in salmon and rockfish. Journal of Parasitology 74, 600–603.CrossRefGoogle Scholar
Devries, A. L. and Cheng, C.-H. (2005). Antifreeze proteins and organismal freezing avoidance in polar fishes. In The Physiology of Polar Fishes (ed. Farrel, A. P. and Steffensen, J. F.), pp. 155–201. Elsevier Academic Press, San Diego, USA.CrossRefGoogle Scholar
Fuse, M., Davey, K. G. and Sommerville, R. I. (1993 a). Osmoregulation in the parasitic nematode Pseudoterranova decipiens. Journal of Experimental Biology 175, 127–142.CrossRefGoogle ScholarPubMed
Fuse, M., Davey, K. G. and Sommerville, R. I. (1993 b). Water compartments and osmoregulation in the parasitic nematode Pseudoterranova decipiens. Journal of Experimental Biology 175, 143–152.CrossRefGoogle ScholarPubMed
Goddard, S. V. and Fletcher, G. L. (1994). Antifreeze proteins – their role in cod survival and distribution from egg to adult. ICES Marine Science Symposium. 198, 676–683.Google Scholar
Gustafson, P. V. (1953). The effect of freezing on encysted Anisakis larvae. Journal of Parasitology 39, 585–588.CrossRefGoogle ScholarPubMed
Heia, K., Lauritzen, K., Nilsen, H., Wold, J. P. and Wedberg, T. (1997). Studies of methods for detection and removal of nematodes in white-fish: x-ray, CT, NMR, time-gating and optical measurements. In Norwegian Institute of Fisheries and Aquaculture research Ltd, Report no. 11. Tromsø, Norway.Google Scholar
Jagdale, G. B. and Grewal, P. S. (2003). Acclimation of entomopathogenic nematodes to novel temperatures: trehalose accumulation and the acquisition of thermotolerance. International Journal for Parasitology 33, 145–152. doi: 10.1016/s0020-7519(02)00257-6.CrossRefGoogle ScholarPubMed
Jagdale, G. B., Grewal, P. S. and Salminen, S. (2005). Both heat-shock and cold-shock influence trehalose metabolism in an entomopathogenic nematode. Journal of Parasitology 91, 988–994.CrossRefGoogle Scholar
Jensen, T. and Idas, K. (1992). Infection with Pseudoterranova decipiens (Krabbe, 1878) larvae in cod (Gadus morhua) relative to proximity of seal colonies. Sarsia 76, 227–230.CrossRefGoogle Scholar
Karl, H. (2008). Nematode larvae in fish on the German market 20 years of consumer related research. Archiv für Lebensmittelhygiene 59, 107–116. doi: 10.2376/0003-925x-59-107.Google Scholar
Kassai, T., Delcampillo, M. C., Euzeby, J., Gaafar, S., Hiepe, T. and Himonas, C. A. (1988). Standardized nomenclature of animal parasitic diseases (snoapad). Veterinary Parasitology 29, 299–326.CrossRefGoogle ScholarPubMed
Koie, M., Berland, B. and Burt, M. D. B. (1995). Development to 3rd-stage larvae occurs in the eggs of Anisakis simplex and Pseudoterranova decipiens (nematoda, ascaridoidea, anisakidae). Canadian Journal of Fisheries and Aquatic Sciences 52, 134–139.CrossRefGoogle Scholar
Magill, S. H. and Sayer, M. D. J. (2004). The effect of reduced temperature and salinity on the blood physiology of juvenile Atlantic cod. Journal of Fish Biology 64, 1193–1205. doi: 10.1111/j.1095-8649.2004.00383.x.CrossRefGoogle Scholar
Margolis, L. (1977). Public-health aspects of codworm infection – review. Journal of the Fisheries Research Board of Canada 34, 887–898.CrossRefGoogle Scholar
McClelland, G., Misra, R. K. and Marcogliese, D. J. (1983). Variations in abundance of larval anisakines sealworm Phocanema decipiens and related species in cod and flatfish from the southern gulf of St Lawrence and the Breton Shelf Canada. Canadian Technical Report of Fisheries and Aquatic Sciences III-51.Google Scholar
Pickup, J. (1990 a). Seasonal variation in the cold hardiness of 3 species of free-living antarctic nematodes. Functional Ecology 4, 257–264.CrossRefGoogle Scholar
Pickup, J. (1990 b). Seasonal-variation in the cold-hardiness of a free-living predatory antarctic nematode, Coomansus gerlachei (monochidae). Polar Biology 10, 307–315.CrossRefGoogle Scholar
Pickup, J. (1990 c). Strategies of cold-hardiness in 3 species of antarctic dorylaimid nematodes. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 160, 167–173.CrossRefGoogle Scholar
Valdimarsson, G., Einarsson, H. and King, F. J. (1985). Detection of parasites in fish muscle by candling technique. Journal of the Association of Official Analytical Chemists 68, 549–551.Google Scholar
Vali, G. (1995). Principles of ice nucleation. In Biological Ice Nucleation and its Applications (ed. JrLee, R. R., Warren, G. J. and Gusta, L. V.), pp. 1–28. APS Press, St Paul, Minnesota, USA.Google Scholar
Wharton, D. A. (1995). Cold tolerance strategies in nematodes. Biological Reviews of the Cambridge Philosophical Society 70, 161–185.CrossRefGoogle ScholarPubMed
Wharton, D. A. and Aalders, O. (2002). The response of Anisakis larvae to freezing. Journal of Helminthology 76, 363–368.CrossRefGoogle ScholarPubMed
Wharton, D. A. (2003). The environmental physiology of Antarctic terrestrial nematodes: a review. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 173, 621–628. doi: 10.1007/s00360-003-0378-0.CrossRefGoogle ScholarPubMed