Abstract
The protozoan parasite Histomonas meleagridis is the causative agent of histomonosis, a poultry disease whose significance is underlined by the absence of any licenced prophylaxis or treatment. Considering the parasite-bacteria interplay, histomonosis represents an intriguing interaction in medicine. The present review targets the molecular research on H. meleagridis, covering the period after re-emergence of histomonosis at the beginning of the twenty-first century until today, from early phylogenetic studies to recent investigations applying omics techniques.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- CP:
-
cysteine peptidase
- FBA:
-
fructose bisphosphate aldolase
- GAPDH:
-
glyceraldehyde-3-phospate dehydrogenase
- MW:
-
molecular weight
- pI:
-
isoelectric point
- TPI:
-
triosephosphate isomerase
References
Amin, A., Nobauer, K., Patzl, M., Berger, E., Hess, M., & Bilic, I. (2012). Cysteine peptidases, secreted by Trichomonas gallinae, are involved in the cytopathogenic effects on a permanent chicken liver cell culture. PLoS ONE, 7, e37417.
Bilic, I. & Hess, M. (2020). Interplay between Histomonas meleagridis and bacteria: mutualistic or predator-prey?. Trends Parasitol, 36(3), 232–235. https://doi.org/10.1016/j.pt.2019.12.015. Epub 2020 Jan 22.
Bilic, I., Leberl, M., & Hess, M. (2009). Identification and molecular characterization of numerous Histomonas meleagridis proteins using a cDNA library. Parasitology, 136, 379–391.
Bilic, I., Jaskulska, B., Souillard, R., Liebhart, D., & Hess, M. (2014). Multi-locus typing of Histomonas meleagridis isolates demonstrates the existence of two different genotypes. PLoS ONE, 9(3), e92438.
Bleyen, N., De, G. K., De, G. J., & Goddeeris, B. M. (2007). Specific detection of Histomonas meleagridis in turkeys by a PCR assay with an internal amplification control. Veterinary Parasitology, 143, 206–213.
Cepicka, I., Hampl, V., & Kulda, J. (2010). Critical taxonomic revision of Parabasalids with description of one new genus and three new species. Protist, 161, 400–433.
Clark, S., & Kimminau, E. (2017). Critical review: Future control of blackhead disease (Histomoniasis) in Poultry. Avian Diseases, 61, 281–288.
Doll, J. P., & Franker, C. K. (1963). Experimental histomoniasis in gnotobiotic turkeys. I. Infection and histopathology of the bacteria-free host. Journal of Parasitology, 49, 411–414.
Ganas, P., Liebhart, D., Glosmann, M., Hess, C., & 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.
Gerbod, D., Edgcomb, V. P., Noel, C., Zenner, L., Wintjens, R., Delgado-Viscogliosi, P., et al. (2001). Phylogenetic position of the trichomonad parasite of turkeys, Histomonas meleagridis (Smith) Tyzzer, inferred from small subunit rRNA sequence. Journal of Eukaryotic Microbiology, 48, 498–504.
Gonzalez-Miguel, J., Morchon, R., Siles-Lucas, M., & Simon, F. (2015). Fibrinolysis and proliferative endarteritis: two related processes in chronic infections? The model of the blood-borne pathogen Dirofilaria immitis. PLoS ONE, 10, e0124445.
Gonzalez-Miguel, J., Siles-Lucas, M., Kartashev, V., Morchon, R., & Simon, F. (2016). Plasmin in parasitic chronic infections: Friend or foe? Trends in Parasitology, 32, 325–335.
Grabensteiner, E., & Hess, M. (2006). PCR for the identification and differentiation of Histomonas meleagridis, Tetratrichomonas gallinarum and Blastocystis spp. Veterinary Parasitology, 142, 223–230.
Grafl, B., Weise, H., Le, B. J., Liebhart, D., Bilic, I., & Hess, M. (2015). Aberrant clinical appearance and pathomorphology noticed during an outbreak of Histomonosis indicates a different pathogenesis of Histomonas meleagridis genotype 2. Avian Diseases, 59, 452–458.
Gruber, J., Ganas, P., & Hess, M. (2017). 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. Parasitology, 144, 1253–1263.
Hafez, H. M., Hauck, R., Luschow, D., & McDougald, L. (2005). Comparison of the specificity and sensitivity of PCR, nested PCR, and real-time PCR for the diagnosis of histomoniasis. Avian Diseases, 49, 366–370.
Hauck, R., & Hafez, H. M. (2009). Partial sequence of the beta-tubulin of Histomonas meleagridis and the activity of benzimidazoles against H. meleagridis in vitro. Parasitology Research, 104, 1183–1189.
Hauck, R., & Hafez, H. M. (2010). Systematic position of Histomonas meleagridis based on four protein genes. Journal of Parasitology, 96, 396–400.
Hauck, R., Luschow, D., & Hafez, H. M. (2006). Detection of Histomonas meleagridis DNA in different organs after natural and experimental infections of meat turkeys. Avian Diseases, 50, 35–38.
Hernandez-Cuevas, N. A., Jhingan, G. D., Petropolis, D., Vargas, M., & Guillen, N. (2019). Acetylation is the most abundant actin modification in Entamoeba histolytica and modifications of actin’s amino-terminal domain change cytoskeleton activities. Cellular Microbiology, 21, e12983.
Hess, M., Grabensteiner, E., & Liebhart, D. (2006a). Rapid transmission of the protozoan parasite Histomonas meleagridis in turkeys and specific pathogen free chickens following cloacal infection with a mono-eukaryotic culture. Avian Pathol, 35, 280–285.
Hess, M., Kolbe, T., Grabensteiner, E., & Prosl, H. (2006b). Clonal cultures of Histomonas meleagridis, Tetratrichomonas gallinarum and a Blastocystis sp. established through micromanipulation. Parasitology, 133, 547–554.
Hess, M., Liebhart, D., Grabensteiner, E., & 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.
Hess, M., Liebhart, D., Bilic, I., & Ganas, P. (2015). Histomonas meleagridis—New insights into an old pathogen. Veterinary Parasitology, 208, 67–76.
Hirt, R. P., de Miguel, N., Nakjang, S., Dessi, D., Liu, Y. C., Diaz, N., et al. (2011). Trichomonas vaginalis pathobiology new insights from the genome sequence. Advances in Parasitology, 77, 87–140.
Kang, S., Tice, A. K., Spiegel, F. W., Silberman, J. D., Panek, T., Cepicka, I., et al. (2017). Between a pod and a hard test: The deep evolution of amoebae. Molecular Biology and Evolution, 34, 2258–2270.
Klodnicki, M. E., McDougald, L. R., & Beckstead, R. B. (2013). A genomic analysis of Histomonas meleagridis through sequencing of a cDNA library. J Parasitol, 99, 264–269.
Lama, A., Kucknoor, A., Mundodi, V., & Alderete, J. F. (2009). Glyceraldehyde-3-phosphate dehydrogenase is a surface-associated, fibronectin-binding protein of Trichomonas vaginalis. Infection and Immunity, 77, 2703–2711.
Leberl, M., Hess, M., & Bilic, I. (2010). Histomonas meleagridis possesses three alpha-actinins immunogenic to its hosts. Molecular and Biochemical Parasitology, 169, 101–107.
Liebhart, D., Weissenbock, H., & Hess, M. (2006). In-situ hybridization for the detection and identification of Histomonas meleagridis in tissues. Journal of comparative pathology, 135, 237–242.
Liebhart, D., Ganas, P., Sulejmanovic, T., & Hess, M. (2017). Histomonosis in poultry: previous and current strategies for prevention and therapy. Avian Pathology, 46, 1–18.
Ma’ayeh, S. Y., Liu, J., Peirasmaki, D., Hornaeus, K., Bergstrom, L. S., Grabherr, M., et al. (2017). Characterization of the Giardia intestinalis secretome during interaction with human intestinal epithelial cells: The impact on host cells. PLoS Neglected Tropical Diseases, 11, e0006120.
Malik, S. B., Brochu, C. D., Bilic, I., Yuan, J., Hess, M., Logsdon, J. M., et al. (2011). Phylogeny of parasitic parabasalia and free-living relatives inferred from conventional markers versus Rpb1, a single-copy gene. PLoS One, 6, e20774.
Mantini, C., Dalia-Cornette, J., Noda, S., van der Heijden, H. M., Capron, M., Dei-Cas, E., et al. (2009). Molecular identification and phylogenetic relationships of trichomonad isolates of galliform birds inferred from nuclear small subunit rRNA gene sequences. Parasitology Research, 106, 163–170.
Mazet, M., Diogon, M., Alderete, J. F., Vivares, C. P., & Delbac, F. (2008). First molecular characterisation of hydrogenosomes in the protozoan parasite Histomonas meleagridis. International Journal for Parasitology, 38, 177–190.
Mazumdar, R., Endler, L., Monoyios, A., Hess, M., & Bilic, I. (2017). Establishment of a de novo reference transcriptome of Histomonas meleagridis reveals basic insights about biological functions and potential pathogenic mechanisms of the parasite. Protist, 168, 663–685.
Mazumdar, R., Nobauer, K., Hummel, K., Hess, M., & Bilic, I. (2019). Molecular characterization of Histomonas meleagridis exoproteome with emphasis on protease secretion and parasite-bacteria interaction. PLoS ONE, 14, e0212429.
McDougald, L. R. (2005). Blackhead disease (histomoniasis) in poultry: A critical review. Avian Diseases, 49, 462–476.
Miles, L. A., & Parmer, R. J. (2013). Plasminogen receptors: The first quarter century. Seminars in Thrombosis and Hemostasis, 39, 329–337.
Monoyios, A., Patzl, M., Schlosser, S., Hess, M., & Bilic, I. (2017). Unravelling the differences: comparative proteomic analysis of a clonal virulent and an attenuated Histomonas meleagridis strain. International Journal for Parasitology. https://doi.org/10.1016/j.ijpara.2017.08.017.
Monoyios, A., Hummel, K., Nobauer, K., Patzl, M., Schlosser, S., Hess, M., et al. (2018). An alliance of gel-based and gel-free proteomic techniques displays substantial insight into the proteome of a virulent and an attenuated Histomonas meleagridis Strain. Front Cell Infect Microbiol, 8, 407.
Pham, A. D., Mast, J., De Gussem, J. K., Mcdougald, L. R., & Goddeeris, B. M. (2013). Establishing mono-eukaryotic Histomonas meleagridis cultures from in vivo infection contaminated with Tetratrichomonas gallinarum and Blastocystis spp. Parasitology, 140, 1266–1274.
Pham, A. D., Mast, J., Magez, S., Goddeeris, B. M., & Carpentier, S. C. (2016). The enrichment of Histomonas meleagridis and its pathogen-specific protein analysis: A first step to shed light on its virulence. Avian Diseases, 60, 628–636.
Regmi, P. R., Shaw, A. L., Hungerford, L. L., Messenheimer, J. R., Zhou, T., Pillai, P., et al. (2016). Regulatory considerations for the approval of drugs against histomoniasis (blackhead disease) in Turkeys, chickens, and game birds in the United States. Avian Diseases, 60, 725–730.
Singh, A., Weissenbock, H. & Hess, M. (2007). Histomonas meleagridis: Immunohistochemical localization of parasitic cells in formalin-fixed, paraffin-embedded tissue sections of experimentally infected turkeys demonstrates the wide spread of the parasite in its host. Exp Parasitol.
Sulejmanovic, T., Grafl, B., Bilic, I., Jaskulska, B., & Hess, M. (2019a). PCR and serology confirm the infection of turkey hens and their resilience to histomonosis in mixed flocks following high mortalities in toms. Parasit Vectors, 12, 228.
Sulejmanovic, T., Turblin, V., Bilic, I., Jaskulska, B., & Hess, M. (2019b). Detection of Histomonas meleagridis DNA in dust samples obtained from apparently healthy meat turkey flocks without effect on performance. Avian Pathology, 48, 329–333.
Tyzzer, E. E. (1919). Developmental phases of protozoon of “blackhead” in turkeys. The Journal of Medical Research, 40, 1–30.
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.
Tyzzer, E. E. (1934). Studies in histomoniasis, or blackhead infection, in chicken and the turkey. Proceedings of the American Academy of Arts and Science, 69, 189–264.
van der Heijden, H. M., Landman, W. J., Greve, S., & Peek, R. (2006). Genotyping of Histomonas meleagridis isolates based on Internal Transcribed Spacer-1 sequences. Avian Pathol, 35, 330–334.
Acknowledgements
The authors thank all colleagues from the Clinic for Poultry and Fish Medicine and Christian Doppler Laboratory for Innovative Poultry Vaccines (IPOV) at the Vetmeduni Vienna for their unceasing support. Furthermore, the authors want to thank the Austrian Science Fund (FWF) for the substantial funding of the research on H. meleagridis and histomonosis.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this paper
Cite this paper
Bilic, I., Hess, M. (2020). Histomonas meleagridis Molecular Traits—From Past to Future. In: Guillen, N. (eds) Eukaryome Impact on Human Intestine Homeostasis and Mucosal Immunology. Springer, Cham. https://doi.org/10.1007/978-3-030-44826-4_4
Download citation
DOI: https://doi.org/10.1007/978-3-030-44826-4_4
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-44825-7
Online ISBN: 978-3-030-44826-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)