Hostname: page-component-7dd5485656-tbj44 Total loading time: 0 Render date: 2025-10-30T02:44:55.116Z Has data issue: false hasContentIssue false
  • English
  • Français

Myxozoan transmission via actinospores: new insights into mechanisms and adaptations for host invasion

Published online by Cambridge University Press:  30 July 2007

D. M. KALLERT ,
S. PONADER ,
E. ESZTERBAUER ,
M. EL-MATBOULI  and
W. HAAS
D. M. KALLERT*
Affiliation:
Institute of Zoology, Fish Biology and Fish Diseases, University of Munich, Kaulbachstraße 37, D-80539 Munich, Germany
S. PONADER
Affiliation:
Institute for Zoology I, University Erlangen, Staudtstraße 5, D-91058, Erlangen, Germany
E. ESZTERBAUER
Affiliation:
Veterinary Medical Research Institute, Hungarian Academy of Sciences, Hungária krt 21, H-1143 Budapest, Hungary
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
*
*Corresponding author: Institute of Zoology, Fish Biology and Fish Diseases, University of Munich, Kaulbachstraße 37, D-80539 Munich, Germany. Tel: +49 89 2180 3561. Fax: +49 89 2180 3912. E-mail: kallert@zoofisch.vetmed.uni-muenchen.de
Get access Rights & Permissions [Opens in a new window]

Summary

Various mechanisms that enable and improve transmission success of myxozoan actinospore stages towards fish hosts are described, based upon a combination of experimental data and functional analysis of morphological characters. For this purpose, laboratory-reared actinospores of Myxobolus cerebralis, Myxobolus parviformis, Henneguya nuesslini and Myxobolus pseudodispar were employed to exemplarily investigate aspects of host attachment and invasion. The process of polar filament discharge of M. cerebralis actinospores was analysed, showing that full discharge occurs in less than 10 msec. Additionally, a mechanism that rapidly contracts the discharged filament after discharge is described for the first time. Its purpose is most likely to bring the actinospore apex rapidly into intimate contact with the surface of the host. Unlike M. cerebralis, M. parviformis actinospores did not discharge polar filaments after mechanical and chemical stimulation, suggesting a different mode of triggering. For H. nuesslini actinospores, experimental results indicated that polar filament discharge is independent of external calcium-ion concentration but is influenced by osmolality. After attachment of an actinospore and prior to penetration into the host, an ensheathed unit (‘endospore’), containing the sporoplasm, was emitted from the valves in a manner which varied from species to species. Experimentally induced sporoplasm emission was time-dependent and was found to be independent of polar filament discharge in H. nuesslini. Remarkably, it could be concluded that the sporoplasm is able to recognize host-stimuli while still within the intact spore. An updated summary of the sequential course of events during host recognition and invasion by actinospores is given.

Keywords

MyxozoaMyxobolus cerebralispolar capsule dischargeactinosporehost invasionsporoplasm

Information

Type
Research Article
Information
Parasitology , Volume 134 , Issue 12 , November 2007 , pp. 1741 - 1750
Copyright
Copyright © Cambridge University Press 2007

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.)

Article purchase

Temporarily unavailable

References

REFERENCES

Belem, A. M. and Pote, L. (2001). Portals of entry and systemic localization of proliferative gill disease organisms in channel catfish Ictalurus punctatus. Diseases of Aquatic Organisms 48, 37–42.CrossRefGoogle ScholarPubMed
Cannon, Q. and Wagner, E. (2003). Comparison of discharge mechanisms of cnidarian cnidae and myxozoan polar capsules. Reviews in Fisheries Science 11, 185–219.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.CrossRefGoogle ScholarPubMed
Holzer, A. S., Sommerville, C. and Wootten, R. (2003). Tracing the route of Sphaerospora truttae from the entry locus to the target organ of the host, Salmo salar L., using an optimized and specific in situ hybridization technique. Journal of Fish Diseases 26, 647–655.CrossRefGoogle Scholar
Janiszewska, J. (1955). Actinomyxidia. Morphology, ecology, history of investigations, systematics, development. Acta Parasitologica Polonica 2, 405–443.Google Scholar
Kallert, D. M., El-Matbouli, M. and Haas, W. (2005 a). Polar filament discharge of Myxobolus cerebralis actinospores is triggered by combined non-specific mechanical and chemical cues. Parasitology 131, 609–616. DOI: 10.1017/S0031182005008383CrossRefGoogle ScholarPubMed
Kallert, D. M., Eszterbauer, E., El-Matbouli, M., Erséus, C. and Haas, W. (2005 b). The life cycle of Henneguya nuesslini Schuberg & Schröder 1905 (Myxozoa) involves a triactinomyxon-type actinospore. Journal of Fish Diseases 28, 71–79. DOI: 10.1111/j.1365-2761.2004.00599.xCrossRefGoogle ScholarPubMed
Kallert, D. M., Eszterbauer, E., Erséus, C., El-Matbouli, M. and Haas, W. (2005 c). Life cycle studies of Myxobolus parviformis sp.n. from bream. Diseases of Aquatic Organisms 66, 233–243.CrossRefGoogle ScholarPubMed
Kawaii, S., Yamashita, K., Nakai, N. and Fusetani, N. (1997). Intracellular calcium transients during nematocyst discharge in Actinulae of the hydroid, Tubularia mesembryanthemum. Journal of Experimental Zoology 278, 299–307.3.0.CO;2-K>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: 10.1368/1066-5234(2001)048[0395:RAIOKO]2.0.CO;2CrossRefGoogle ScholarPubMed
Longshaw, M., Le Deuff, R. M., Harris, A. F. and Feist, S. W. (2002). Development of proliferative kidney disease in rainbow trout, Oncorhynchus mykiss (Walbaum), following short-term exposure to Tetracapsula bryosalmonae infected bryozoans. Journal of Fish Diseases 25, 443–449.CrossRefGoogle Scholar
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. DOI: 10.1577/1548-8667(1992)004<0044:EIWDID>2.3.CO;22.3.CO;2>CrossRefGoogle Scholar
Meier-Brook, C. (1978). Calcium uptake by Marisa cornuarietis (Gastropoda; Ampulariidae), a predator of schistosome-bearing snails. Archiv für Hydrobiologie 82, 449–464.Google Scholar
Morris, D. J., Adams, A. and Richards, R. H. (2000). In situ hybridisation identifies the gill as a portal of entry for PKX (Phylum Myxozoa), the causative agent of proliferative kidney disease in salmonids. Parasitology Research 86, 950–956.CrossRefGoogle Scholar
Russell, R. J. and Watson, G. M. (1995). Evidence for intracellular stores of calcium ions involved in regulating nematocyst discharge. Journal of Experimental Zoology 273, 175–185.CrossRefGoogle Scholar
Santoro, G. and Salleo, A. (1991). The discharge of in situ nematocysts of the acontia of Aiptasia mutabilis is a Ca2+-induced response. Journal of Experimental Biology 156, 173–185.CrossRefGoogle Scholar
Uspenskaya, A. V. (1982). New data on the life cycle and biology of Myxosporidia. Archiv für Protistenkunde 126, 309–338.CrossRefGoogle Scholar
Xiao, C. and Desser, S. S. (2000). The longevity of 7 forms of actinosporean spores from oligochaetes of Lake Sasajewun, Algonquin Park, Ontario, and their reaction to fish mucus. Journal of Parasitology 86, 193–195. DOI: 10.1645/0022-3395(2000)086[0193:TLOASF]2.0.CO;2CrossRefGoogle ScholarPubMed
Yokoyama, H. (2003). A review: Gaps in our knowledge on Myxozoan parasites of fishes. Fish Pathology (Gyobio Kenkyu) 38, 125–136.CrossRefGoogle Scholar
Yokoyama, H. and Urawa, S. (1997). Fluorescent labelling of actinospores for determining the portals of entry into fish. Diseases of Aquatic Organisms 30, 165–169. DOI: 10.1023/A:1005752913780CrossRefGoogle Scholar
Yokoyama, H., Ogawa, K. and Wakabayashi, H. (1991). A new collection method of actinosporeans – a probable infective stage of myxosporeans to fishes – from tubificids and experimental infection of goldfish with the actinosporean, Raabeia sp. Fish Pathology (Gyobio Kenkyu) 26, 133–138.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., Kim, H. J. and Urawa, S. (2006). Differences in host selection of two myxosporeans, Myxobolus arcticus and Thelohanellus hovorkai. Journal of Parasitology 92, 725–729. DOI: 10.1645/GE-831R.1CrossRefGoogle ScholarPubMed