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Molecular characterization of five Sarcocystis species in red deer (Cervus elaphus), including Sarcocystis hjorti n. sp., reveals that these species are not intermediate host specific

Published online by Cambridge University Press:  07 December 2009

STINA S. DAHLGREN  and
BJØRN GJERDE
STINA S. DAHLGREN*
Affiliation:
Norwegian School of Veterinary Science, Department of Food Safety and Infection Biology, Section of Microbiology, Immunology and Parasitology, P.O. Box 8146 Dep., 0033 Oslo, Norway
BJØRN GJERDE
Affiliation:
Norwegian School of Veterinary Science, Department of Food Safety and Infection Biology, Section of Microbiology, Immunology and Parasitology, P.O. Box 8146 Dep., 0033 Oslo, Norway
*
*Corresponding author: Tel: +47 22 96 49 68. Fax: +47 22 96 49 65. E-mail: [email protected]
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Summary

Muscle tissue from 37 red deer from Norway was examined for sarcocysts. Sarcocysts from 2 reindeer were obtained for comparative studies. Cysts were excised and morphologically classified by light microscopy, scanning electron microscopy, and DNA sequence analysis. Five Sarcocystis species, Sarcocystis hjorti n. sp., Sarcocystis hardangeri, Sarcocystis ovalis, Sarcocystis rangiferi, and Sarcocystis tarandi, were found. All 5 species have previously been identified from either reindeer or moose by their sarcocyst morphology and/or ssu rRNA gene sequence. S. hjorti was the most prevalent species. Multiple variants of the ssu rRNA gene and the first internal transcribed spacer were found in S. rangiferi and S. tarandi from both red deer and reindeer. Phylogenetic analyses indicated that S. tarandi occurs in both red deer and reindeer, but it could not be clearly demonstrated whether the sequence variation within S. rangiferi between hosts was due to different paralogues or/and different species. DNA sequencing was necessary for definitive species identification, since the hair-like protrusions on the cysts of S. hjorti were not always recognizable by light microscopy and since different cervids harbour Sarcocystis species with highly similar cyst morphology of which at least some are not intermediate host specific.

Keywords

Sarcocystisred deerssu rRNA geneITS-1
Type
Research Article
Information
Parasitology , Volume 137 , Issue 5 , April 2010 , pp. 815 - 840
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Bergmann, V. and Kinder, E. (1976). Elektronenmikroskopische Untersuchungen zur Wandstruktur von Sarkozysten in der Skelettmuskulatur von Wildschwein und Reh. Monatshefte für Veterinärmedizin 31, 785–788.Google Scholar
Blažek, K., Schramlova, J., Ippen, R. and Kotrly, A. (1978). Die Sarkosporidiose des Rehwildes (Capreolus capreolus L.). Folia Parasitologica 25, 99–102.Google ScholarPubMed
Chen, X. W., Zuo, Y. X. and Hu, J. J. (2003). Experimental Sarcocystis hominis infection in a water buffalo (Bubalus bubalis). Journal of Parasitology 89, 393–394. doi: 10.1645/0022-3395(2003)089[0393:ESHIIA]2.0.CO;2.CrossRefGoogle Scholar
Colwell, D. D. and Mahrt, J. L. (1981). Ultrastructure of the cyst wall and merozoites of Sarcocystis from moose (Alces alces) in Alberta, Canada. Zeitschrift für Parasitenkunde 65, 317–329. doi: 10.1007/BF00926727.CrossRefGoogle Scholar
Dahlgren, S. S. and Gjerde, B. (2007). Genetic characterisation of six Sarcocystis species from reindeer (Rangifer tarandus tarandus) in Norway based on the small subunit rRNA gene. Veterinary Parasitology 146, 204–213. doi: 10.1016/j.vetpar.2007.02.023.CrossRefGoogle ScholarPubMed
Dahlgren, S. S. and Gjerde, B. (2008). Sarcocystis in moose (Alces alces): molecular identification and phylogeny of six Sarcocystis species in moose, and a morphological description of three new species. Parasitology Research 103, 93–110. doi: 10.1007/s00436-008-0936-1.CrossRefGoogle Scholar
Dahlgren, S. S. and Gjerde, B. (2009). Sarcocystis in Norwegian roe deer (Capreolus capreolus): molecular and morphological identification of Sarcocystis oviformis n. sp. and Sarcocystis gracilis and their phylogenetic relationship with other Sarcocystis species. Parasitology Research 104, 993–1003. doi: 10.1007/s00436-008-1281-0.CrossRefGoogle Scholar
Dahlgren, S. S., Gjerde, B., Skirnisson, K. and Gudmundsdottir, B. (2007). Morphological and molecular identification of three species of Sarcocystis in reindeer (Rangifer tarandus tarandus) in Iceland. Veterinary Parasitology 149, 191–198. doi: 10.1016/j.vetpar.2007.08.015.CrossRefGoogle ScholarPubMed
Dubey, J. P. (1982). Development of ox-coyote cycle of Sarcocystis cruzi. Journal of Protozoology 29, 591–601. doi: 10.1111/j.1550-7408.1982.tb05448.xGoogle ScholarPubMed
Dubey, J. P. and Lozier, S. M. (1983). Sarcocystis infection in the white-tailed deer (Odocoileus virginianus) in Montana: intensity and description of Sarcocystis odoi n sp. American Journal of Veterinary Research 44, 1738–1743.Google ScholarPubMed
Dubey, J. P. and Speer, C. A. (1985). Prevalence and ultrastructure of three types of Sarcocystis in mule deer, Odocoileus hemionus (Rafinesque), in Montana. Journal of Wildlife Diseases 21, 219–228.CrossRefGoogle ScholarPubMed
Dubey, J. P. and Speer, C. A. (1986). Sarcocystis infections in mule deer (Odocoileus hemionus) in Montana and the descriptions of three new species. American Journal of Veterinary Research 47, 1052–1055.Google ScholarPubMed
Dubey, J. P., Speer, C. A., Callis, G. and Blixt, J. A. (1982). Development of the sheep-canid cycle of Sarcocystis tenella. Canadian Journal of Zoology 60, 2464–2477. doi: 10.1139/z82-315.CrossRefGoogle Scholar
Dubey, J. P., Jolley, W. R. and Thorne, T. T. (1983). Sarcocystis sybillensis sp. nov. from the North American elk (Cervus elaphus). Canadian Journal of Zoology 61, 737–742. doi: doi:10.1139/z83-098.CrossRefGoogle Scholar
Dubey, J. P., Speer, C. A. and Fayer, R. (1989). Stucture and lifecycle. In Sarcocystosis of Animals and Man. pp. 2–13. CRC Press, Boca Raton, FL, USA.Google Scholar
Entzeroth, R. (1982). A comparative light and electron microscope study of the cysts of Sarcocystis species of roe deer (Capreolus capreolus). Zeitschrift für Parasitenkunde 66, 281–292. doi: 10.1007/BF00925345.CrossRefGoogle ScholarPubMed
Entzeroth, R. (1985). Light-, scanning-, and transmission electron microscope study of the cyst wall of Sarcocystis gracilis Rátz, 1909 (Sporozoa, Coccidia) from the roe deer (Capreolus capreolus L.). Archiv für Protistenkunde 129, 183–186.CrossRefGoogle Scholar
Entzeroth, R., Neméseri, L. and Scholtyseck, E. (1983). Prevalence and ultrastructure of Sarcocystis sp. from the red deer (Cervus elaphus L.) in Hungary. Parasitologia Hungarica 16, 47–52.Google Scholar
Erber, M., Boch, J. and Barth, J. (1978). Drei Sarkosporidienarten des Rehwildes. Berliner und Münchener Tierärztliche Wochenschrift 91, 482–486.Google Scholar
Gestrich, R., Heydorn, O. A. and Baysu, N. (1975 a). Beiträge zum Lebenszyklus der Sarkosporidien. VI. Untersuchungen zur Artendifferenzierung bei Sarcocystis fusiformis und Sarcocystis tenella. Berliner und Münchener Tierärztliche Wochenschrift 88, 191–197.Google ScholarPubMed
Gestrich, R., Mehlhorn, H. and Heydorn, O. A. (1975 b). Licht- und elektronenmikroskopische Untersuchungen an Cysten von Sarcocystis fusiformis in der Muskulatur von Kälbern nach experimenteller Infektion mit Oocysten und Sporocysten der grossen form von Isospora bigemina der Katze. Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene, I. Abteilung Originale A 233, 261–276.Google Scholar
Gjerde, B. (1984 a). A light microscopic comparison of the cysts of four species of Sarcocystis infecting the domestic reindeer (Rangifer tarandus) in northern Norway. Acta Veterinaria Scandinavica 25, 195–204.CrossRefGoogle ScholarPubMed
Gjerde, B. (1984 b). Sarcocystis infection in wild reindeer (Rangifer tarandus) from Hardangervidda in southern Norway: with a description of the cysts of Sarcocystis hardangeri n. sp. Acta Veterinaria Scandinavica 25, 205–212.CrossRefGoogle ScholarPubMed
Gjerde, B. (1984 c). Sarcocystis hardangeri and Sarcocystis rangi n. sp. from the domestic reindeer (Rangifer tarandus) in northern Norway. Acta Veterinaria Scandinavica 25, 411–418.Google Scholar
Gjerde, B. (1985 a). The fox as a definitive host for Sarcocystis rangi from reindeer (Rangifer tarandus tarandus). Acta Veterinaria Scandinavica 26, 140–142.CrossRefGoogle Scholar
Gjerde, B. (1985 b). Ultrastructure of the cysts of Sarcocystis hardangeri from skeletal muscle of reindeer (Rangifer tarandus tarandus). Canadian Journal of Zoology 63, 2676–2683. doi: 10.1139/z85-400.CrossRefGoogle Scholar
Gjerde, B. (1985 c). Ultrastructure of the cysts of Sarcocystis rangiferi from skeletal muscle of reindeer (Rangifer tarandus tarandus). Canadian Journal of Zoology 63, 2669–2675. doi: 10.1139/z85-399.CrossRefGoogle Scholar
Gjerde, B. (1985 d). Ultrastructure of the cysts of Sarcocystis tarandi from skeletal muscle of reindeer (Rangifer tarandus tarandus). Canadian Journal of Zoology 63, 2913–2918. doi: 10.1139/z85-436.CrossRefGoogle Scholar
Gjerde, B. (1986). Scanning electron microscopy of the sarcocysts of six species of Sarcocystis from reindeer (Rangifer tarandus tarandus). Acta Pathologica, Microbiologica, et Immunologica 94, 309–317.Google ScholarPubMed
Gjerde, B. and Bratberg, B. (1984). The domestic reindeer (Rangifer tarandus) from Northern Norway as intermediate host for three species of Sarcocystis. Acta Veterinaria Scandinavica 25, 195–204.CrossRefGoogle ScholarPubMed
Hernandez-Rodriguez, S., Acosta, I. and Navarrete, I. (1992). Sarcocystis jorrini sp. nov. from the fallow deer Cervus dama. Parasitology Research 78, 557–562. doi: 10.1007/BF00936452.CrossRefGoogle ScholarPubMed
Hernández-Rodríguez, S., Martínez-Gómez, F. and Navarrete, I. (1981 a). Sarcocystis cervicanis, nueva especie del ciervo (Cervus elaphus). Revista Ibérica de Parasitologia 41, 43–51.Google Scholar
Hernández-Rodríguez, S., Martínez-Gómez, F., Navarrete, I. and Acosta-Garcia, I. (1981 b). Estudio al microscopio optico y electronico del quiste de Sarcocystis cervicanis. Revista Ibérica de Parasitologia 41, 351–361.Google Scholar
Heydorn, O. A. (1985). Zur Entwicklung von Sarcocystis arieticanis n. sp. Berliner und Münchener Tierärztliche Wochenschrift 98, 231–241.Google Scholar
Heydorn, O. A. and Unterholzner, J. (1983). Zur Entwicklung von Sarcocystis hircicanis n. sp. Berliner und Münchener Tierärztliche Wochenschrift 96, 275–282.Google ScholarPubMed
Kutkienė, L. (2001). The species composition of European roe deer (Capreolus capreolus) Sarcocystis in Lithuania. Acta Zoologica Lituanica 11, 97–101.CrossRefGoogle Scholar
Kutkienė, L. (2003). Investigations of red deer (Cervus elaphus) Sarcocystis species composition in Lithuania. Acta Zoologica Lituanica 13, 390–395.CrossRefGoogle Scholar
Li, Q. Q., Yang, Z. Q., Zuo, Y. X., Attwood, S. W., Chen, X. W. and Zhang, Y. P. (2002). A PCR-based RFLP analysis of Sarcocystis cruzi (Protozoa: Sarcocystidae) in Yunnan Province, PR China, reveals the water buffalo (Bubalus bubalis) as a natural intermediate host. Journal of Parasitology 88, 1259–1261. doi: 10.1645/0022-3395(2002)088[1259:APBRAO]2.0.CO;2.CrossRefGoogle Scholar
Mehlhorn, H., Heydorn, O. and Gestrich, R. (1975 a). Licht- und elektronenmikroskopische Untersuchungen an Cysten von Sarcocystis fusiformis in der Muskulatur von Kälbern nach experimenteller Infektion mit Oocysten und Sporocysten von Isospora hominis Raillet et Lucet, 1891. Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene, I. Abteilung Originale A 231, 301–322.Google Scholar
Mehlhorn, H., Heydorn, O. and Gestrich, R. (1975 b). Licht- und elektronenmikroskopische Untersuchungen an Cysten von Sarcocystis fusiformis in der Muskulatur von Kälbern nach experimenteller Infektion mit Oocysten und Sporocysten der grossen Form von Isospora bigemina des Hundes. Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene, I. Abteilung Originale A 232, 392–409.Google Scholar
Morrison, D. A., Bornstein, S., Thebo, P., Wernery, U., Kinne, J. and Mattsson, J. G. (2004). The current status of the small subunit rRNA phylogeny of the coccidia (Sporozoa). International Journal for Parasitology 34, 501–514. doi: 10.1016/j.ijpara.2003.11.006.CrossRefGoogle ScholarPubMed
Mullaney, T., Murphy, A. J., Kiupel, M., Bell, J. A., Rossano, M. G. and Mansfield, L. S. (2005). Evidence to support horses as natural intermediate hosts for Sarcocystis neurona. Veterinary Parasitology 133, 27–36. doi: 10.1016/j.vetpar.2005.05.016.CrossRefGoogle ScholarPubMed
Narisawa, A., Yokoi, S., Kawai, K., Sakui, M. and Sugawara, K. (2008). Sarcocystis spp. infection in wild sika deer (Cervus nippon yesoensis). Journal of the Japan Veterinary Medical Association 61, 321–323.CrossRefGoogle Scholar
Odening, K., Stolte, M., Walter, G. and Bockhardt, I. (1994). The European badger (Carnivora:Mustelidae) as intermediate host of further three Sarcocystis species (Sporozoa). Parasite 1, 23–30.Google Scholar
Odening, K. (1998). The present state of species-systematics in Sarcocystis Lankester, 1982 (Protista, Sporozoa, Coccidia). Systematic Parasitology 41, 209–233. doi: 10.1023/A:1006090232343CrossRefGoogle Scholar
Pacheco, N. D., Sheffield, H. G. and Fayer, R. (1978). Fine structure of immature cysts of Sarcocystis cruzi. Journal of Parasitology 2, 320–325.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818. doi: 10.1093/bioinformatics/14.9.817.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574. doi: 10.1093/bioinformatics/btg180.CrossRefGoogle ScholarPubMed
Rosenthal, B. M., Dunams, D. B. and Pritt, B. (2008). Restricted genetic diversity in the ubiquitous cattle parasite, Sarcocystis cruzi. Infection, Genetics and Evolution 8, 588–592. doi: 10.1016/j.meegid.2008.04.004.Google Scholar
Saito, M., Itagaki, T., Shibata, Y. and Itagaki, H. (1995). Morphology and experimental definitive hosts of Sarcocystis sp. from sika deer, Cervus nippon centralis, in Japan. Japanese Journal of Parasitology 44, 218–221.Google Scholar
Saito, M., Shibata, Y., Kobayashi, T., Kobayashi, M., Kubo, M. and Itagaki, H. (1996). Ultrastructure of the cyst wall of Sarcocystis species with canine final host in Japan. The Journal of Veterinary Medical Science 58, 861–867.CrossRefGoogle ScholarPubMed
Schramlová, J. and Blažek, K. (1978). Ultrastruktur der Cystenwand der Sarcosporidien des Rehes (Capreolus capreolus L.). Zeitschrift für Parasitenkunde 55, 43–48.CrossRefGoogle Scholar
Sedlaczek, J. and Wesemeier, H. H. (1995). On the diagnostics and nomenclature of Sarcocystis species (Sporozoa) in roe deer (Capreolus capreolus). Applied Parasitology 36, 73–82.Google Scholar
Slapeta, J. R., Kyselová, I., Richardson, A. O., Modrý, D. and Lukeš, J. (2002). Phylogeny and sequence variability of the Sarcocystis singaporensis Zaman and Colley, (1975) 1976 ssrDNA. Parasitology Research 88, 810–815. doi: 10.1007/s00436-002-0657-9Google ScholarPubMed
Speer, C. A. and Dubey, J. P. (1982). Sarcocystis wapiti sp. nov. from the North American wapiti (Cervus elaphus). Canadian Journal of Zoology 60, 881–888.Google Scholar
Spickschen, C. and Pohlmeyer, K. (2002). Untersuchung zum Vorkommen von Sarkosporidien bei Reh-, Rot- und Muffelwild in zwei unterschiedlichen Naturräumen des Bundeslandes Niedersachsen. Zeitschrift für Jagdwissenschaft 48, 35–48.Google Scholar
Stolte, M., Bockhardt, I. and Odening, K. (1996). A comparative scanning electron microscopic study of the cyst wall in 11 Sarcocystis species of mammals. Journal of Zoology 239:821–832. doi: 10.1111/j.1469-7998.1998.tb00030.xGoogle Scholar
Stolte, M., Bockhardt, I. and Odening, K. (1997). First report of Sarcocystis rangiferi and a second Sarcocystis species with parasite-induced encapsulation in cervids from Central Europe. Acta Protozoologica 36, 131–135.Google Scholar
Takano, K., Hamada, K., Ogiwara, Y. and Yagi, K. (2006). Phylogenetic analysis of Sarcocystis sp. isolated from muscle of sika deer in Hokkaido by partial 18S rRNA gene sequence. Hokkaido Institute of Public Health 56, 41–44.Google Scholar
Wesemeier, H. H. and Sedlaczek, J. (1995 a). One known Sarcocystis species and two found for the first time in red deer and wapiti (Cervus elaphus) in Europe. Applied Parasitology 36, 245–251.Google Scholar
Wesemeier, H. H. and Sedlaczek, J. (1995 b). One known Sarcocystis species and one found for the first time in fallow deer (Dama dama). Applied Parasitology 36, 299–302.Google ScholarPubMed
Yang, Z. Q., Zuo, Y. X., Yao, Y. G., Chen, X. W., Yang, G. C. and Zhang, Y. P. (2001). Analysis of the 18S rRNA genes of Sarcocystis species suggests that the morphologically similar organisms from cattle and water buffalo should be considered the same species. Molecular and Biochemical Parasitology 115, 283–288. doi: 10.1016/SO166-6851(01)00283-3.Google Scholar
Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. The University of Texas at Austin, USA. (Dissertation).Google Scholar