Abstract
The roe deer (Capreolus capreolus) has been identified as an intermediate host for six known Sarcocystis species, S. capreolicanis, S. entzerothi, S. gracilis, S. linearis, S. oviformis, and S. silva. In this study, we identified Sarcocystis species in the diaphragm and tongue muscles from the Lithuanian and Spanish roe deer, respectively, on the basis of a microscopic examination and DNA analysis. A total of 43 and 27 sarcocysts were isolated and characterized from the Lithuanian and Spanish roe deer, respectively. Overall six Sarcocystis species were identified in roe deer from Lithuania, and only three of them, S. gracilis, S. linearis, and S. silva were found to have infecting animals from Spain. The current paper represents first molecular results of Sarcocystis species in the Spanish roe deer. Furthermore, transmission electron microscopy examination revealed specific wall structure of sarcocysts studied, S. linearis was characterized by ribbon-like villar protrusions (vp) (type 8a), and S. oviformis was distinguished by elongated vp resembling spades or mushroom-like structures (type 39). Based on 18S rDNA and cox1 sequences, Sarcocystis species from the roe deer showed considerable intraspecific genetic variability. However, similar values of intraspecific genetic variation were estimated at both genes analysed. The highest variability was observed for S. capreolicanis and S. linearis in both genes and for S. silva at cox1. Consequently, the level of genetic variability of Sarcocystis from the roe deer varied depending on species rather than on gene analysed or geographical area.
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References
Calero-Bernal R, Verma SK, Cerqueira-Cézar CK, Schafer LM, Van Wilpe E, Dubey JP (2015) Sarcocystis mehlhorni, n. sp. (Apicomplexa: Sarcocystidae) from the black-tailed deer (Odocoileus hemionus columbianus). Parasitol Res 114:4397–4403. https://doi.org/10.1007/s00436-015-4679-5
Dahlgren SS, 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. Parasitol Res 104:993–1003. https://doi.org/10.1007/s00436-008-1281-0
Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R (2016) Sarcocystosis of animals and humans, 2nd edn. CRC Press, Boca Raton
Entzeroth R (1982) A comparative light and electron microscope study of the cysts of Sarcocystis species of roe deer (Capreolus capreolus). Z Parasitenkd 66:281–292. https://doi.org/10.1007/bf00925345
Erber M, Boch J, Barth D (1978) Drei Sarkosporidienarten des Rehwildes. Berl Münch Tierärztl Wochenschr 91:482–486.
Gjerde B (2012) Morphological and molecular characterization and phylogenetic placement of Sarcocystis capreolicanis and Sarcocystis silva n. sp. from roe deer (Capreolus capreolus) in Norway. Parasitol Res 110:1225–1237. https://doi.org/10.1007/s00436-011-2619-6
Gjerde B (2013) Phylogenetic relationships among Sarcocystis species in cervids, cattle and sheep inferred from the mitochondrial cytochrome c oxidase subunit I gene. Int J Parasitol 43:579–591. https://doi.org/10.1016/j.ijpara.2013.02.004
Gjerde B (2014) Sarcocystis species in red deer revisited: with a redescription of two known species as Sarcocystis elongata n. sp. and Sarcocystis truncata n. sp. based on mitochondrial cox1 sequences. Parasitology 141:441–452. https://doi.org/10.1017/S0031182013001819
Gjerde B (2016) Molecular characterisation of Sarcocystis bovifelis, Sarcocystis bovini n. sp., Sarcocystis hirsuta and Sarcocystis cruzi from cattle (Bos taurus) and Sarcocystis sinensis from water buffaloes (Bubalus bubalis). Parasitol Res 115:1473–1492. https://doi.org/10.1007/s00436-015-4881-5
Gjerde B, Giacomelli S, Bianchi A, Bertoletti I, Mondani H, Gibelli LR (2017) Morphological and molecular characterization of four Sarcocystis spp., including Sarcocystis linearis n. sp., from roe deer (Capreolus capreolus) in Italy. Parasitol Res 116:1317–1338. https://doi.org/10.1007/s00436-017-5410-5
Kirillova V, Prakas P, Calero-Bernal R, Gavarāne I, Fernández-García JL, Martínez-González M, Rudaitytė-Lukošienė E, Martínez-Estéllez MÁH, Butkauskas D, Kirjušina M (2018) Identification and genetic characterization of Sarcocystis arctica and Sarcocystis lutrae in red foxes (Vulpes vulpes) from Baltic States and Spain. Parasit Vectors 11:173. https://doi.org/10.1186/s13071-018-2694-y
Kolenda R, Ugorski M, Bednarski M (2014) Molecular characterization of Sarcocystis species from Polish roe deer based on ssu rRNA and cox1 sequence analysis. Parasitol Res 113:3029–3039. https://doi.org/10.1007/s00436-014-3966-x
Kutkienė L (2001) The species composition of European roe deer (Capreolus capreolus) Sarcocystis in Lithuania. Acta Zool Lituanica 11:97–101. https://doi.org/10.1080/13921657.2001.10512363
Kutkienė L, Prakas P, Sruoga A, Butkauskas D (2010) The mallard duck (Anas platyrhynchos) as intermediate host for Sarcocystis wobeseri sp. nov. from the barnacle goose (Branta leucopsis). Parasitol Res 107:879–888. https://doi.org/10.1007/s00436-010-1945-4
López C, Panadero R, Bravo A, Paz A, Sánchez-Andrade R, Díez-Baños P, Morrondo P (2003) Sarcocystis spp. infection in roe deer (Capreolus capreolus) from the north-west of Spain. Z Jagdwiss 49:211–218. https://doi.org/10.1007/bf02189739
Pérez-Creo A, Panadero R, López C, Díaz P, Vázquez L, Díez-Baños P, Morrondo P (2013) Prevalence and identity of Sarcocystis spp. in roe deer (Capreolus capreolus) in Spain: a morphological study. Res Vet Sci 95:1036–1040. https://doi.org/10.1016/j.rvsc.2013.08.003
Prakas P, Butkauskas D, Rudaitytė E, Kutkienė L, Sruoga A, Pūraitė I (2016) Morphological and molecular characterization of Sarcocystis taeniata and Sarcocystis pilosa n. sp from the sika deer (Cervus nippon) in Lithuania. Parasitol Res 115:3021–3032. https://doi.org/10.1007/s00436-016-5057-7
Prakas P, Rudaitytė E, Butkauskas D, Kutkienė L (2017) Sarcocystis entzerothi n. sp. from the European roe deer (Capreolus capreolus). Parasitol Res 116:271–279. https://doi.org/10.1007/s00436-016-5288-7
Prakas P, Kirillova V, Calero-Bernal R, Kirjušina M, Rudaitytė-Lukošienė E, Habela MÁ, Gavarāne I, Butkauskas D (2019) Sarcocystis species identification in the moose (Alces alces) from the Baltic States. Parasitol Res 118:1601–1608. https://doi.org/10.1007/s00436-019-06291-0
Rozas J, Ferrer-Mata A, Sánchez-Del Barrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Rudaitytė-Lukošienė E, Prakas P, Butkauskas D, Kutkienė L, Vepštaitė-Monstavičė I, Servienė E (2018) Morphological and molecular identification of Sarcocystis spp. from the sika deer (Cervus nippon), including two new species Sarcocystis frondea and Sarcocystis nipponi. Parasitol Res 117:1305–1315. https://doi.org/10.1007/s00436-018-5816-8
Rudaitytė-Lukošienė E, Prakas P, Strazdaitė-Žielienė Ž, Servienė E, Januškevičius V, Butkauskas D (2020) Molecular identification of two Sarcocystis species in fallow deer (Dama dama) from Lithuania. Parasitol Int 75:102044. https://doi.org/10.1016/j.parint.2019.102044
Santini S, Mancianti F, Nigro M, Poli A (1997) Ultrastructure of the cyst wall of Sarcocystis sp. in roe deer. J Wildl Dis 33:853–859. https://doi.org/10.7589/0090-3558-33.4.853
Schramlová J, Blazek K (1978) Ultrastruktur der Cystenwand der Sarkosporidien des Rehes (Capreolus capreolus L.). Z Parasitenkd 55:43–48.
Spickschen C, Pohlmeyer K (2002) Untersuchung zum Vorkommen von Sarkosporidien bei Reh-, Rot- und Muffelwild in zwei unterschiedlichen Naturräumen des Bundeslandes Niedersachsen. Z Jagdwiss 48:35–48. https://doi.org/10.1007/bf02285355
Trupkiewicz JG, Calero-Bernal R, Verma SK, Mowery J, Davison S, Habecker P, Georoff TA, Ialeggio DM, Dubey JP (2016) Acute, fatal Sarcocystis calchasi-associated hepatitis in roller pigeons (Columba livia f. dom.) at Philadelphia zoo. Vet Parasitol 216:52–58. https://doi.org/10.1016/j.vetpar.2015.11.008
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This work was supported by the Research Council of Lithuania (grant number S-MIP-17-45) and Open Access to research infrastructure of the Nature Research Centre under Lithuanian open access network initiative.
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Rudaitytė-Lukošienė, E., Delgado de las Cuevas, G.E., Prakas, P. et al. Sarcocystis spp. diversity in the roe deer (Capreolus capreolus) from Lithuania and Spain. Parasitol Res 119, 1363–1370 (2020). https://doi.org/10.1007/s00436-020-06603-9
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DOI: https://doi.org/10.1007/s00436-020-06603-9