Hostname: page-component-84b7d79bbc-dwq4g Total loading time: 0 Render date: 2024-07-27T23:51:44.206Z Has data issue: false hasContentIssue false
  • English
  • Français

Polar filament discharge of Myxobolus cerebralis actinospores is triggered by combined non-specific mechanical and chemical cues

Published online by Cambridge University Press:  22 July 2005

D. M. KALLERT ,
M. EL-MATBOULI  and
W. HAAS
D. M. KALLERT
Affiliation:
Institute for Zoology I, University Erlangen, Staudtstrasse 5 D-91058, Erlangen, Germany
M. EL-MATBOULI
Affiliation:
Institute of Zoology, Fish Biology and Fish Diseases, University of Munich, Kaulbachstraße 37, D-80539 Munich, Germany
W. HAAS
Affiliation:
Institute for Zoology I, University Erlangen, Staudtstrasse 5 D-91058, Erlangen, Germany
Get access Rights & Permissions [Opens in a new window]

Abstract

This study presents initial evidence for the requirement of both chemical and mechanical stimuli to discharge polar capsules of Myxobolus cerebralis actinospores, the causative agent of salmonid whirling disease. The obligate need for combined discharge triggers was concluded from data obtained in a before/after experimental set-up carried out with individual locally immobilized actinospores. Homogenized rainbow trout mucus as chemostimulus and tangency of the apical region of the spores to achieve mechanical stimulation were applied subsequently. The actinospores showed discharged polar filaments exclusively when mucus substrate application was followed by touching the polar capsule-bearing region, but not when either stimulus was offered solely to the same individuals. We measured filament discharge rates to mucus preparations in a microscopic assay using supplementary vibration stimuli to ensure mechanical excitation. The actinospores responded similarly to different frequencies, which suggested a touch-sensitive recognition mechanism. Discharge specificity for salmonid mucus could not be confirmed, as mucus of common carp and bream could trigger similar filament expulsion rates. To a lesser extent homogenized frog epidermis and bovine submaxillary mucin could also stimulate the attachment reaction. In contrast, mucus of a pulmonate freshwater snail elicited no response.

Keywords

MyxozoaMyxobolus cerebralispolar capsule dischargechemo-perceptionhost specificitymucus
Type
Research Article
Information
Parasitology , Volume 131 , Issue 5 , November 2005 , pp. 609 - 616
Copyright
© 2005 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

Anderson, C. L., Okamura, B. and Canning, E. U. ( 1998). Hox genes confirm that Myxozoa are extremely reduced triploblasts. Nature, London 392, 346–347.CrossRefGoogle Scholar
Browne, R. K., Scheltinga, D. M., Pomering, M. and Mahony, M. ( 2002). Testicular myxosporidiasis in anurans, with a description of Myxobolus fallax n. sp. Systematic Parasitology 52, 97–110. DOI: 10.1023/A:1015609513809.CrossRefGoogle Scholar
Canning, E. U. and Okamura, B. ( 2004). Biodiversity and evolution of the Myxozoa. Advances in Parasitology 56, 43–131. DOI: 10.1016/S0065-308(03)56002-X.CrossRefGoogle Scholar
Cannon, Q. and Wagner, E. ( 2003). Comparison of discharge mechanisms of cnidarian Cnidae and myxozoan polar capsules. Reviews in Fisheries Science 11, 185–219. DOI: 10.1080/10641260390244305.CrossRefGoogle Scholar
Dapson, R. W. ( 1970). Histochemistry of mucus in the skin of the frog, Rana pipiens. Anatomical Record 166, 615–626.CrossRefGoogle Scholar
Denny, M. ( 1983). Molecular biomechanics of molluscan mucous secretions. In The Mollusca Vol. 1. ( ed. Hochachka, P. W.), pp. 431–465. Academic Press, New York.CrossRef
El-Matbouli, M., Fischer-Scherl, T. and Hoffmann, R. W. ( 1992). Present knowledge of the life cycle, taxonomy, pathology, and therapy of some Myxosporea spp. Important for freshwater fish. Annual Review of Fish Diseases, 367–402.CrossRefGoogle Scholar
El-Matbouli, M., Hoffmann, R. W., Schoel, H., McDowell, T. S. and Hedrick, R. P. ( 1999). Whirling disease: host specificity and interaction between the actinosporean stage of Myxobolus cerebralis and rainbow trout Oncorhynchus mykiss. Diseases of Aquatic Organisms 35, 1–12.Google Scholar
Gilbert, M. A. and Granath, W. O. ( 2003). Whirling disease of salmonid fish: life cycle, biology, and disease. Journal of Parasitology 89, 658–667.CrossRefGoogle Scholar
Haas, W. ( 1975). Einfluss von CO2 und pH auf das Fixationsverhalten der Cercarie von Diplostomum spathaceum (Trematoda). Zeitschrift für Parasitenkunde 46, 53–60.CrossRefGoogle Scholar
Haas, W. ( 2003). Parasitic worms: Strategies for host-finding, recognition and invasion. Zoology 106, 349–364.CrossRefGoogle Scholar
Haas, W. and Haberl, B. ( 1997). Host recognition by trematode miracidia and cercariae. In Advances in Trematode Biology ( ed. Fried, B. and Graczyk, T. K.), pp. 197–227. CRC Press, Boaca Raton, FL, USA.
Haas, W., Haberl, B., Hofmann, M., Kerschensteiner, S. and Ketzer, U. ( 1999). Ichthyophtirius multifiliis invasive stages find their fish hosts with complex behaviour patterns and in response to different chemical signals. European Journal of Protistology 35, 129–135.CrossRefGoogle Scholar
Haas, W., Stiegeler, P., Keating, A., Kullmann, B., Rabenau, H., Schönamsgruber, E. and Haberl, B. ( 2002). Diplostomum spathaceum cercariae respond to a unique profile of cues during recognition of their fish host. International Journal for Parasitology 32, 1145–1154. DOI: 10.1016/S0020-7519(02)00089-9.CrossRefGoogle Scholar
Hedrick, R. P., El-Matbouli, M., Adkison, M. A. and MacConnell, E. ( 1998). Whirling disease: re-emergence among wild trout. Immunological Reviews 166, 365–376.CrossRefGoogle Scholar
Hoffman, G. L. ( 1990). Myxobolus cerebralis, a worldwide cause of salmonid whirling disease. Journal of Aquatic Animal Health 2, 30–37.2.3.CO;2>CrossRefGoogle Scholar
Ibragimov, A. ( 2001). Polar filaments of Myxobolus pseudodispar spores. Tsitologiia 43, 742–746.Google Scholar
Kalbe, M., Haberl, B. and Haas, W. ( 2000). Finding of the snail host by Fasciola hepatica and Trichobilharzia ocellata: Compound analysis of ‘Miracidia attracting glycoprotein’. Experimental Parasitology 96, 231–242. DOI: 10.1006/expr.2000.4579.CrossRefGoogle Scholar
Kass-Simon, G. and Hufnagel, L. A. ( 1992). Suspected chemoreceptors in coelenterates and ctenophores. Microscopy Research Technique 22, 265–284.CrossRefGoogle Scholar
Kearn, G. C. ( 1967). Experiments on host-finding and host specificity in the monogean skin parasite Entobdella soleae. Parasitology 57, 585–605.CrossRefGoogle Scholar
Kent, M. L., Andree, K. B., Bartholomew, J. L., El-Matbouli, M., Desser, S. S., Devlin, R. H., Feist, S. W., Hedrick, R. P., Hoffmann, R. W., Khattra, J., Hallett, S. L., Lester, R. J. G., Longshaw, M., Palenzeula, O., Siddall, M. E. and Xiao, C. ( 2001). Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48, 395–413. DOI: 10.1043/1066-5234(2001)048<0395:RAIOKO>2.0.CO;2.2.0.CO;2>CrossRefGoogle Scholar
Lom, J. ( 1990). Phylum Myxozoa. In Handbook of Protoctista ( ed. Margulis, L., Corliss, J. O., Melkonian, M. and Chapman, D. J.), pp. 36–52. Jones and Bartlett Publishers, Boston.
Markiw, M. E. ( 1992). Experimentally induced whirling disease II. Determination of longevity of the infective triactinomyxon stage of Myxobolus cerebralis by vital staining. Journal of Aquatic Animal Health 4, 44–47.Google Scholar
McGeorge, J., Sommerville, C. and Wootten, R. ( 1997). Studies of actinosporean myxozoan stages parasitic in oligochaetes from the sediments of a hatchery where Atlantic salmon harbour Sphaerospora truttae infection. Diseases of Aquatic Organisms 30, 107–119.CrossRefGoogle Scholar
Monsigny, M., Petit, C. and Roche, A. C. ( 1988). Colorimetric determinatipon of neutral sugars by a resorcinol sulfuric acid micromethod. Analytical Biochemistry 175, 525–530.CrossRefGoogle Scholar
Okamura, B., Curry, A., Wood, T. S. and Canning, E. U. ( 2002). Ultrastructure of Buddenbrockia identifies it as a myxozoan and verifies the bilaterian origin of the Myxozoa. Parasitology 124, 215–223. DOI: 10.1017/S0031182001001184.CrossRefGoogle Scholar
Ozer, A. and Wootten, R. ( 2002). Biological characteristics of some actinosporeans. Journal of Natural History 36, 2199–2209.CrossRefGoogle Scholar
Schlegel, M., Lom, J., Stechmann, A., Bernhard, D., Leipe, D., Dyková, I. and Sogin, M. L. ( 1996). Phylogenetic analysis of complete small subunit ribosomal RNA coding region of Myxidium lieberkuehni: evidence that Myxozoa are Metazoa related to the Bilateria. Archiv für Protistenkunde 147, 1–9.CrossRefGoogle Scholar
Siddall, M. E., Martin, D. S., Bridge, D., Desser, S. S. and Cone, D. K. ( 1995). The demise of a phylum of protists: phylogeny of myxozoa and other parasitic cnidaria. Journal of Parasitology 8, 961–967.CrossRefGoogle Scholar
Uspenskaya, A. V. ( 1995). Alteration of actinosporean and myxosporean phases in the life cycle of Zschokkella nova (myxozoa). Journal of Eukaryotic Microbiology 42, 665–668.CrossRefGoogle Scholar
Wagner, E. ( 2001 a). Triactinomyxon polar filament discharge: effects of mucus, magnetic fields, and MS-222. The Ichtyogram 12 Issue 1, 6–7.Google Scholar
Wagner, E. ( 2001 b). Effect of calcium chelators, proline, and glutathione on polar filament extrusion of tractinomyxons of Myxobolus cerebralis. The Ichtyogram 12 Issue 2, 5–8.Google Scholar
Watson, G. M. and Hessinger, D. A. ( 1987). Receptor-mediated endocytosis of a chemoreceptor involved in triggering the discharge of cnidae in a sea anemone tentacle. Tissue and Cell 19, 747–755.CrossRefGoogle Scholar
Xiao, C. and Desser, S. S. ( 2000). Molecular characterization of myxozoan parasites from Lake Sasajewun, Algonquin Park, Ontario, by riboprinting. Journal of Eukaryotic Microbiology 47, 85–89. DOI: 10.1043/1066-5234(2000)047<0085:MCOMPF>2.0.CO;2.2.0.CO;2>CrossRefGoogle Scholar
Yokoyama, H., Ogawa, K. and Wakabayashi, H. ( 1993). Some biological characteristics of actinosporeans from the oligochaete Branchiura sowerbyi. Diseases of Aquatic Organisms 17, 223–228.CrossRefGoogle Scholar
Yokoyama, H., Ogawa, K. and Wakabayashi, H. ( 1995). Myxobolus cultus n. Sp. (Myxosporea: Myxobolidae) in goldfish Carassius auratus transformed from the actinosporean stage in the oligochaete Branchiura sowerbyi. Journal of Parasitology 81, 446–451.Google Scholar
Yokoyama, H., Danjo, T., Ogawa, K. and Wakabayashi, H. ( 1997). A vital staining technique with fluorescein diacetate (FDA) and propidium iodide (PI) for the determination of viability of myxosporean and actinosporean spores. Journal of Fish Diseases 20, 281–286. DOI: 10.1046/j.1365-2761.1997.00293.X.CrossRefGoogle Scholar
Yokoyama, H. ( 2003). A review: gaps in our knowledge on myxozoan parasites of fishes. Fish Pathology 38, 125–136.CrossRefGoogle Scholar