Hostname: page-component-6d856f89d9-76ns8 Total loading time: 0 Render date: 2024-07-16T06:12:24.510Z Has data issue: false hasContentIssue false
  • English
  • Français

Long-term in vitro cultivation of Histomonas meleagridis coincides with the dominance of a very distinct phenotype of the parasite exhibiting increased tenacity and improved cell yields

Published online by Cambridge University Press:  08 May 2017

JANINE GRUBER ,
PETRA GANAS  and
MICHAEL HESS
JANINE GRUBER
Affiliation:
Christian Doppler Laboratory for Innovative Poultry Vaccines (IPOV), University of Veterinary Medicine Vienna, Vienna, Austria
PETRA GANAS
Affiliation:
Christian Doppler Laboratory for Innovative Poultry Vaccines (IPOV), University of Veterinary Medicine Vienna, Vienna, Austria
MICHAEL HESS*
Affiliation:
Christian Doppler Laboratory for Innovative Poultry Vaccines (IPOV), University of Veterinary Medicine Vienna, Vienna, Austria Clinic for Poultry and Fish Medicine, Department for Farm Animals and Veterinary Public Health, University of Veterinary Medicine Vienna, Vienna, Austria
*
*Corresponding author: Clinic for Poultry and Fish Medicine, University of Veterinary Medicine Vienna, Veterinärplatz 1, A-1210 Vienna, Austria. E-mail: michael.hess@vetmeduni.ac.at
Get access Rights & Permissions [Opens in a new window]

Summary

The majority of research on Histomonas meleagridis was performed in the first half of the last century, especially those on morphological aspects. In the present study identical monoxenic settings for cultures of the same H. meleagridis clonal strain in its virulent low passage and attenuated high passage form enabled a comparative analysis of parasite characteristics. For the first time, it could be shown that long-term in vitro cultivation led to a severe shift in cell morphology, with the occurrence of a very distinct phenotype expressing a flagellated and highly amoebic cell morphology. Furthermore, the attenuated parasites showed better growth rates and a higher tenacity when confronted with adverse conditions. During these experiments up to 100% of the parasites, both virulent and attenuated, assumed a completely rounded morphology elucidated by electron microscopy. The findings indicate that such previously reported cyst-like stages are a defence strategy of H. meleagridis, independent of the passage level in vitro and pathogenicity in vivo. In conclusion, long-term in vitro passaging of H. meleagridis led not only to an attenuation of the parasite, as previously demonstrated, but also to a shift in the parasite's phenotype regarding morphology, growth behaviour and a higher level of tenacity.

Keywords

Histomonas meleagridismorphologyflagellain vitro growthtenacitycysts
Type
Research Article
Information
Parasitology , Volume 144 , Issue 9 , August 2017 , pp. 1253 - 1263
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Bishop, A. (1938). Histomonas meleagridis in domestic fowls (Gallus gallus). Cultivation and experimental infection. Parasitology 30, 181–194.Google Scholar
BonDurant, R. H. and Wakenell, P. S. (1994). Histomonas meleagridis and relatives. In Parasitic protozoa, Vol. 9 (ed. Kreier, J. P.), 189–206. Academic Press, New York, USA.Google Scholar
Borges, F. B., Gottardi, B., Stuepp, C., Larré, A. B., Vieira, P. B., Tasca, T. and Carli, G. A. (2007). Morphological aspects of Monocercomonas sp. and investigation on probable pseudocysts occurrence. Parasitology Research 101, 1503.Google Scholar
Delappe, I. P. (1952). Studies on Histomonas meleagridis. I. Use of antibiotics to facilitate in vitro isolation. Experimental Parasitology 2, 79–86.CrossRefGoogle Scholar
DeVolt, H. M. and Davis, C. R. (1936). Blackhead (infectious enterohepatitis) in turkeys, with notes on other intestinal protozoa. Agricultural Experiment Station, University of Maryland, College Park, MD., Bulletin 392, 493–567.Google Scholar
Dwyer, D. (1970). An improved method for cultivating Histomonas meleagridis . Journal of Parasitology 56, 191–192.CrossRefGoogle ScholarPubMed
Franker, C. K. and Doll, J. P. (1964). Experimental histomoniasis in gnotobiotic turkeys. II. Effects of some cecal bacteria on pathogenesis. Journal of Parasitology 50, 636–640.Google Scholar
Friedhoff, K. T., Kuhnigk, C. and Müller, I. (1991). Experimental infections in chickens with Chilomastix gallinarum, Tetratrichomonas gallinarum and Tritrichomonas eberthi . Parasitology Research 77, 329–334.Google Scholar
Ganas, P., Liebhart, D., Glösmann, M., Hess, C. and Hess, M. (2012). Escherichia coli strongly supports the growth of Histomonas meleagridis, in a monoxenic culture, without influence on its pathogenicity. International Journal for Parasitology 42, 893–901.Google Scholar
Gerhold, R. W., Lollis, L. A., Beckstead, R. B. and McDougald, L. R. (2010). Establishment of culture conditions for survival of Histomonas meleagridis in Transit. Avian Diseases 54, 948–950.Google Scholar
Granger, B. L., Warwood, S. J., Benchimol, M. and De Souza, W. (2000). Transient invagination of flagella by Tritrichomonas foetus . Parasitology Research 86, 699–709.CrossRefGoogle ScholarPubMed
Harrison, A. P. Jr., Hansen, P. A., DeVolt, H. M., Holst, A. P. and Tromba, F. G. (1954). Studies on the pathogenesis of infectious enterohepatitis (blackhead) of turkeys. Poultry Science 33, 84–93.CrossRefGoogle Scholar
Hauck, R., Armstrong, P. and McDougald, L. (2010). Histomonas meleagridis (Protozoa, Trichomonadidae): analysis of growth requirements in vitro . Journal of Parasitology 96, 1–7.CrossRefGoogle ScholarPubMed
Hess, M., Kolbe, T., Grabensteiner, E. and Prosl, H. (2006). Clonal cultures of Histomonas meleagridis, Tetratrichomonas gallinarum and a Blastocystis sp. established through micromanipulation. Parasitology 133, 547–554.Google Scholar
Hess, M., Liebhart, D., Grabensteiner, E. and Singh, A. (2008). Cloned Histomonas meleagridis passaged in vitro resulted in reduced pathogenicity and is capable of protecting turkeys from histomonosis. Vaccine 26, 4187–4193.CrossRefGoogle ScholarPubMed
Hess, M., Liebhart, D., Bilic, I. and Ganas, P. (2015). Histomonas meleagridis – new insights into an old pathogen. Veterinary Parasitology 208, 67–76.CrossRefGoogle ScholarPubMed
Honigberg, B. M. and Bennett, C. J. (1971). Lightmicroscopic observations on structure and division of Histomonas meleagridis (Smith). Journal of Protozoology 18, 687–697.Google Scholar
Jeelani, G., Sato, D., Husain, A., Escueta-de Cadiz, A., Sugimoto, M., Soga, T., Suematsu, M. and Nozaki, T. (2012). Metabolic profiling of the protozoan parasite Entamoeba invadens revealed activation of unpredicted pathway during Encystation. PLoS ONE 7, e37740.Google Scholar
Lee, D., Long, P., Millard, B. and Bradley, J. (1969). The fine structure and method of feeding of the tissue parasitizing stages of Histomonas meleagridis . Parasitology 59, 171–184.Google Scholar
Liebhart, D., Windisch, M. and Hess, M. (2010). Oral vaccination of 1-day-old turkeys with in vitro attenuated Histomonas meleagridis protects against histomonosis and has no negative effect on performance. Avian Pathology 39, 399–403.Google Scholar
Liebhart, D., Ganas, P., Sulejmanovic, T. and Hess, M. (2017). Histomonosis in poultry: previous and current strategies for prevention and therapy. Avian Pathology 46, 1–18.Google Scholar
Lund, E. E. (1963). Histomonas wenrichii n. sp. (Mastigophora: Mastigamoebidae), a nonpathogenic parasite of gallinaceous birds. Journal of Protozoology 10, 401–404.Google Scholar
Lund, E. E., Augustine, P. C. and Ellis, D. J. (1966). Immunizing action of in vitro-attenuated Histomonas meleagridis in chickens and turkeys. Experimental Parasitology 18, 403–407.Google Scholar
Lund, E. E., Augustine, P. C. and Chute, A. M. (1967). Histomonas meleagridis after one thousand in vitro passages. Journal of Protozoology 14, 349–351.Google Scholar
McDougald, L. R. and Reid, W. M. (1978). Histomonas meleagridis and relatives. Parasitic Protozoa 2, 139–161.Google Scholar
Mielewczik, M., Mehlhorn, H., Al-Quraishy, S., Grabensteiner, E. and Hess, M. (2008). Transmission electron microscopic studies of stages of Histomonas meleagridis from clonal cultures. Parasitology Research 103, 745–750.CrossRefGoogle ScholarPubMed
Munasinghe, V. S. (2016). New discovery and ultrastructural description of Dientamoeba fragilis cysts and the establishment of an animal model for their study. Doctoral thesis. http://hdl.handle.net/10453/44195.Google Scholar
Munasinghe, V. S., Vella, N. G., Ellis, J. T., Windsor, P. A. and Stark, D. (2013). Cyst formation and faecal–oral transmission of Dientamoeba fragilis–the missing link in the life cycle of an emerging pathogen. International Journal for Parasitology 43, 879–883.Google Scholar
Munsch, M., Lotfi, A., Hafez, H. M., Al-Quraishy, S. and Mehlhorn, H. (2009). Light and transmission electron microscopic studies on trophozoites and cyst-like stages of Histomonas meleagridis from cultures. Parasitology Research 104, 683–689.Google Scholar
Osada, M. (1959). Electron-microscopic studies on protozoa. The Keio Journal of Medicine 8, 99–108.Google Scholar
Pereira-Neves, A., Ribeiro, K. C. and Benchimol, M. (2003). Pseudocysts in trichomonads–new insights. Protist 154, 313–329.Google Scholar
Schuster, F. L. (1968). Ultrastructure of Histomonas meleagridis (Smith) Tyzzer, a parasitic amebo-flagellate. Journal of Parasitology 54, 725–737.CrossRefGoogle Scholar
Stark, D., Garcia, L. S., Barratt, J. L. N., Phillips, O., Roberts, T., Marriott, D., Harkness, J. and Ellis, J. T. (2014). Description of Dientamoeba fragilis cyst and precystic forms from human samples. Journal of Clinical Microbiology 52, 2680–2683.Google Scholar
Tyzzer, E. E. (1919). Developmental phases of the protozoan of “Blackhead” in turkeys. Journal of Medical Research 40, 1–30.Google Scholar
Tyzzer, E. E. (1920). The flagellate character and reclassification of the parasite producing “Blackhead” in turkeys: Histomonas (Gen. nov.) meleagridis (Smith). Journal of Parasitology 6, 124–131.Google Scholar
Van der Heijden, H. M., McDougald, L. R. and Landman, W. J. (2005). High yield of parasites and prolonged in vitro culture of Histomonas meleagridis . Avian Pathology 34, 505–508.Google Scholar
Wenrich, D. H. (1943). Observations on the morphology of Histomonas (Protozoa, Mastigophora) from pheasants and chickens. Journal of Morphology 72, 279–303.Google Scholar
Wheatley, W. (1951). A rapid staining procedure for intestinal amoebae and flagellates. American Journal of Clinical Pathology 21, 990–991.Google Scholar
Zaragatzki, E., Hess, M., Grabensteiner, E., Abdel-Ghaffar, F., Al-Rasheid, K. A. S. and Mehlhorn, H. (2010 a). Light and transmission electron microscopic studies on the encystation of Histomonas meleagridis . Parasitology Research 106, 977–983.CrossRefGoogle ScholarPubMed
Zaragatzki, E., Mehlhorn, H., Abdel-Ghaffar, F., Al-Rasheid, K. A. S., Grabensteiner, E. and Hess, M. (2010 b). Experiments to produce cysts in cultures of Histomonas meleagridis – the agent of histomonosis in poultry. Parasitology Research 106, 1005–1007.Google Scholar
Zeibig, E. (2004). Clinical Parasitology: a Practical Approach, Vol. 2. Elsevier Saunders, Philadelphia, USA.Google Scholar
Supplementary material: File

Gruber supplementary material

Figures S1-S2

Download Gruber supplementary material(File)
File 1.4 MB