Abstract
A total of 57 tissue samples of domestic pigs (Sus scrofa) were collected from the meat outlets of five north Indian states and examined for sarcocystosis by histological and molecular methods. The genomic DNA extracted from five representative positive isolates was subjected to PCR amplification of the partial 18S rRNA gene followed by cloning and sequencing. Sequence analysis of the newly generated Indian isolates recorded 96.9–100.0% identity with published sequences of Sarcocystis suihominis. Two new haplotypes that have not been previously described manifested 99.5–100.0% nucleotide homology within themselves. In the phylogenetic analysis, Indian isolates of S. suihominis grouped together with S. suihominis originating from Italy, and they collectively formed a sister clade with Sarcocystis miescheriana within a clade containing various Sarcocystis spp. of ruminants having felids as final hosts. At the same time, this clade separated from a sister clade containing Sarcocystis spp. of bovid or cervid ruminants using canids as known or surmised definitive host. The current study established the phylogenetic relationship of Indian isolates of S. suihominis with various Sarcocystis spp. as well as with other taxa of Sarcocystidae family based on 18S rRNA gene for the first time.
Similar content being viewed by others
References
Agnihotri RK, Juyal PD, Bhatia BB (1987) Microsarcocysts in pigs in Uttar Pradesh, India. J Vet Parasitol 1:69–70
Avapal RS, Bhatia BB, Sharma JK, Juyal PD (2002) Seroprevalence of Sarcocystis in swine. J Parasit Dis 18:75–76
Avapal RS, Sharma JK, Juyal PD (2004) Pathological changes in Sarcocystis infection in domestic pigs (Sus scrofa). Vet J 168:358–361
Banerjee PS (1998) Studies on pathogenesis of Sarcocystis tenella in sheep. J Vet Parasitol 12:65
Banerjee PS, Bhatia BB, Pandit BA (1994) Sarcocystis suihominis infection in human beings in India. J Vet Parasitol 8:57–58
Barrows PL, Prestwood AK, Green CE (1982) Experimental Sarcocystis suicanis infections: disease in growing pigs. Am J Vet Res 43:1409–1412
Caspari K, Grimm F, Kuhn N, Caspari NC, Basso W (2011) First report of naturally acquired clinical sarcocystosis in a pig breeding stock. Vet Parasitol 177:175–178
Claveria FG, De La Pena C, Cruz-Flores MJ (2001) Sarcocystis miescheriana infection in domestic pigs (Sus scrofa) in the Philipines. J Parasitol 87:938–939
Daugschies A (2006) Protozoeninfektionen des Schweines. In: Schnieder (Ed.), Veterinärmedizinische Parasitologie. Parey, Stuttgart, Germany 365-367
Daugschies A, Altfeld E, Rommel M (1989) Hemostatic alterations in pigs fed sublethal doses of Sarcocystis miescheriana. Vet Parasitol 34:1–13
Devault A, Banuls AL (2008) The promastigote surface antigen gene family of the Leishmania parasite: differential evolution by positive selection and recombination. BMC Evol Biol 8:292
Dubey JP (1976) A review of Sarcocystis of domestic animals and of other coccidia of cats and dogs. J Am Vet Med Assoc 169:1061–1078
Dubey JP, Speer CA, Fayer R (1989) Sarcocystosis of animals and man. CRC Press
Dubey J, Calero-Bernal R, Rosenthal B, Speer C, Fayer R (2016) Sarcocystosis of animals and humans. 2nd ed: Taylor and Francis Group: CRC Press
Fischer S, Odening K (1998) Characterization of bovine Sarcocystis species by analysis of their 18S ribosomal DNA sequences. J Parasitol 84:50–54
Franssen F, Bilska-Zając E, Deksne G, Sprong H, Pozio E, Rosenthal B, Rozycki M, Van Der Giessen J (2015) Genetic evidence of interspecies introgression of mitochondrial genomes between Trichinella spiralis and Trichinella britovi under natural conditions. Infect Genet Evol 36:323–332
Frenkel JK, Heydorn AO, Mehlhorn H, Rommel M (1979) Sarcocystinae: Nomina dubia and available names. Z Parasitenkd 58:115–139
Gazzonis AL, Gjerde B, Villa L, Minazzi S, Zanzani SA, Riccaboni P, Sironi G, Manfredi MT (2019) Prevalence and molecular characterisation of Sarcocystis miescheriana and Sarcocystis suihominis in wild boars (Sus scrofa) in Italy. Parasitol Res 118:1271–1287
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
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
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
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
Gupta SL, Gautam OP (1984) Sarcocystis infection in pigs of Hissar, Haryana, India and its transmission to dogs. Vet Parasitol 16:1–3
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hu JJ, Wen T, Chen XW, Liu TT, Esch GW, Huang S (2016) Prevalance, morphology, and molecular characterization of Sarcocystis heydorni sarcocysts from cattle (Bos taurus) in China. J Parasitol 102:545–548
Huang Z, Ye Y, Zhang H, Deng S, Tao J, Hu J, Yang Y (2019) Morphological and molecular characterizations of Sarcocystis miescheriana and Sarcocystis suihominis in domestic pigs (Sus scrofa) in China. Parasitol Res 118:3491–3496
Kaur M, Singh BB, Sharma R, Gill JP (2016) Pervasive environmental contamination with human feces results in high prevalence of zoonotic Sarcocystis infection in pigs in the Punjab, India. J Parasitol 102:229–232
Kia EB, Mirhendi H, Rezaeian M, Zahabiun F, Sharbatkhori M (2011) First molecular identification of Sarcocystis miescheriana (Protozoa, Apicomplexa) from wild boar (Sus scrofa) in Iran. Exp Parasitol 127:724–726
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549
Li QQ, Yang ZQ, Zuo YX, Attwood SW, Chen XW, Zhang YP (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. J Parasitol 88:1259–1261
Mehlhorn H, Heydorn AO (1977) Light and electron microscopic studies of Sarcocystis suihominis. 1. The development of cysts in experimentally infected pigs. Zentralbl Bakteriol Orig A 239:124–139
Moré G, Schares S, Maksimov A, Conraths FJ, Venturini MC, Schares G (2013) Development of a multiplex real time PCR to differentiate Sarcocystis spp. affecting cattle. Vet Parasitol 197:85–94
Motamedi GR, Dalimi A, Nouri A, Aghaeipour K (2011) Ultrastructural and molecular characterization of Sarcocystis isolated from camel (Camelus dromedarius) in Iran. Parasitol Res 108:949–954
Mu J, Myers RA, Jiang H, Liu S, Ricklefs S, Waisberg M, Chotivanich K, Wilairatana P, Krudsood S, White NJ, Udomsangpetch R (2010) Plasmodium falciparum genome-wide scans for positive selection, recombination hot spots and resistance to antimalarial drugs. Nat Genet 42:268–271
Neefs JM, Van De Peer Y, De Ruk P, Agoris, De Wachter R (1991) Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 19:1987–2016
Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press
Omata Y, Heydorn AO, Heidrich HG, Igarashi I, Saito A, Toba H, Suzuki N (1993) Survey of Sarcocystis spp. infection in slaughtered pigs in East Hokkaido, Japan. J Protozool Res 3:29–30
Prasanth H (1995) Sarcocystis infection in domestic pigs in Uttar Pradesh. Vet Parasitol 9:119–123
Prasanth H, Bhatia BB (1996) On the species of Sarcocystis of pigs in Uttar Pradesh, India with a description of a sarcocyst of hitherto unrecognized species. J Vet Parasitol 10:57–61
Saleque A, Bhatia BB (1991) Prevalence of Sarcocystis in domestic pigs in India. Vet Parasitol 40:151–153
Singh BB, Sharma R, Sharma JK, Juyal PD (2010) Parasitic zoonoses in India: an overview. Rev Sci Tech Off Int Epiz 29:629–637
Solanki PK, Shrivastava HO, Shah HL (1991) Prevalence of Sarcocystis in naturally infected pigs in Madhya Pradesh with an epidemiological explanation for the higher prevalence of Sarcocystis suihominis. Indian J Anim Sci 61:820–821
Soulsby EJL (1982) Helminths, arthropods and protozoa of domesticated animals, 7th ed. Bailliere Tindal 684-685
Tenter AM (1995) Current research on Sarcocystis species of domestic animals. Int J Parasitol 25:1311–1330
Tenter AM, Johnson AM (1997) Phylogeny of the tissue cyst-forming coccidia. Adv Parasitol 39:69–139
Yan W, Qian W, Li X, Wang T, Ding K, Huang T (2013) Morphological and molecular characterization of Sarcocystis miescheriana from pigs in the central region of China. Parasitol Res 112:975–980
Yang ZQ, Zuo YX, Yao YG, Chen XW, Yang GC, Zhang YP (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. Mol Biochem Parasitol 115:283–288
Acknowledgements
Authors are thankful to the Director, ICAR-IVRI, Izatnagar for the facilities provided.
Funding
This work was supported by ICAR-IVRI, Izatnagar for the project entitled “Surveillance and characterization of pork associated zoonotic parasites with special reference to Trichinella spp. (Project No. IVRI/PARA/14-17-004).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Panagiotis Karanis
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Chauhan, R.P., Kumari, A., Nehra, A.K. et al. Genetic characterization and phylogenetic analysis of Sarcocystis suihominis infecting domestic pigs (Sus scrofa) in India. Parasitol Res 119, 3347–3357 (2020). https://doi.org/10.1007/s00436-020-06857-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-06857-3