Abstract
The trichomonads form part of the phylum Parabasalia, a complex assemblage of diverse species of flagellated protists, with some members recognized as pathogens of men and/or animals. Associations, probably as commensals, between the species Tetratrichomonas ovis and sheep were reported in North America during the 1960s based on morphological and cultural characteristics. Intriguingly, no subsequent studies of this topic have been published. Feces, collected from sheep (n = 55) and goats (n = 14), reared on small-scale, production facilities in Southeastern Brazil, were examined for parabasalids. Protozoa, demonstrating morphologies and motility characteristic of trichomonads, were detected by direct microscopy in 64% of sheep and 43% of goat samples. In contrast to T. ovis, none of the samples could be cultured in Diamond’s medium; however, cultures were obtained for three goat and seventeen sheep samples in peptonized broth. Based on morphological analyses, all isolates were classified as members of the genus Tetratrichomonas. Sequencing of the ITS1-5.8S rRNA gene-ITS2 region revealed three highly similar genotypes that were essentially identical to sequences reported for Tetratrichomonas spp. isolated from the preputial cavity of cattle in the USA and Southern Brazil. The findings of this study extend and enhance our knowledge of parasitism in small ruminants by parabasalids.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amin A, Neubauer C, Liebhart D, Grabensteiner E, Hess M (2010) Axenization and optimization of in vitro growth clonal cultures of Tetratrichomonas gallinarum and Trichomonas gallinae. Exp Parasitol 124:202–208. https://doi.org/10.1016/j.exppara.2009.09.014
Andersen FL, Levine ND, Hammomd DM (1962) The morphology of Trichomonas ovis from the cecum of domestic sheep. J Parasitol 48:589–595
Andrews J, Johnson CM, Schwartz SC (1933) The use of fecal extracts in the cultivation of Endamoeba histolytica. Am J Trop Med Hyg 13:591–593
Bezerra MJG, Kim PCP, Moraes ÉP, Sá SG, Albuquerque PPF, Silva JG, Alves BHS, Mota RA (2015) Detection of Toxoplasma gondii in the milk of naturally infected goats in the Northeast of Brazil. Transbound Emerg Dis 62:421–424. https://doi.org/10.1111/tbed.12160
Bittencourt MV, Meneses IDS, Ribeiro-Andrade M, de Jesus RF, de Araújo FR, Gondim LFP (2016) Sarcocystis spp. in sheep and goats: frequency of infection and species identification by morphological, ultrastructural, and molecular tests in Bahia, Brazil. Parasitol Res 115:1683–1689. https://doi.org/10.1007/s00436-016-4909-5
Brugerolle G (1976) Cytologie ultrastructurale, systematique et evolutiondes Trichomonadida. Annla Stn Biol Besse-en Chandesse 10:1–57
Burgess SL, Gilchrist CA, Lynn TC, Petri WA (2017) Parasitic protozoa and interactions with the host intestinal microbiota. Infect Immun 85:01–12. https://doi.org/10.1128/IAI.00101-17
Castella J, Munoz E, Ferrer D, Gutierrez J (1997) Isolation of the trichomonad Tetratrichomonas buttreyi (Hibler et al., 1960) Honigberg, 1963 in bovine diarrhoeic faeces. Vet Parasitol 70:41–45. https://doi.org/10.1016/S0304-4017(96)01140-5
Cepicka I, Hampl V, Kulda J, Flegr J (2006) New evolutionary lineages, unexpected diversity, and host specificity in the parabasalid genus Tetratrichomonas. Mol Phylogenet Evol 39:542–551. https://doi.org/10.1016/j.ympev.2006.01.005
Cisak E, Zając V, Sroka J, Sawczyn A, Kloc A, Dutkiewicz J, Wójcik-Fatla A (2017) Presence of pathogenic Rickettsiae and protozoan in samples of raw milk from cows, goats, and sheep. Foodborne Pathog Dis 14:189–194. https://doi.org/10.1089/fpd.2016.2203
Cobo ER, Campero CM, Mariante RM, Benchimol M (2011) Ultrastructural study of a tetratrichomonad species isolated from prepucial smegma of virgin bulls. Vet Parasitol 117:195–211. https://doi.org/10.1016/j.vetpar.2003.07.026
Collántes-Fernández E, Fort MC, Ortega-Mora LM (2018) In: Schares G (ed) Trichomonas in parasitic protozoa of farm animals and pets. Springer, Cham, pp 313–388
Damboriarena PA, Silveira CS, Morais RM, Anjos BL (2016) Natural Sarcocystis gigantea infection in sheep from Southern Brazil. Cienc Rural 46:1229–1232. https://doi.org/10.1590/0103-8478cr20151183
Diamond LS (1957) The establishment of various trichomonads of animals and man in axenic cultures. J Parasitol 43:488–490
Dimasuay KG, Rivera WL (2013) Molecular characterization of trichomonads isolated from animal hosts in the Philippines. Vet Parasitol 23:289–295. https://doi.org/10.1016/j.vetpar.2013.03.019
Dos Santos CSD, Jesus VLT, Mcintosh D, Berto BP, Lopes CWG (2015) Co-infection by Tritrichomonas foetus and Pentatrichomonas hominis in asymptomatic cats. Pesqui Vet Bras 35:980–988. https://doi.org/10.1590/S0100-736X2015001200007
Dos Santos CS, De Jesus VLT, Mcintosh D, Carreiro CC, Batista LCO, do Bomfim Lopes B, Lopes CWG (2017) Morphological, ultrastructural, and molecular characterization of intestinal tetratrichomonads isolated from non-human primates in southeastern Brazil. Parasitol Res 116:2479–2488. https://doi.org/10.1007/s00436-017-5552-5
Dybicz M, Perkowski K, Baltaza W, Padzik M, Sędzikowska A, Chomicz L (2018) Molecular identification of Trichomonas tenax in the oral environment of domesticated animals in Poland–potential effects of host diversity for human health. Ann Agric Environ Med 25:464–468. https://doi.org/10.26444/aaem/92309
Emameh RZ, Purmonen S, Sukura A, Parkkila S (2018) Surveillance and diagnosis of zoonotic foodborne parasites. Food Sci Nutr 6:3–17. https://doi.org/10.1002/fsn3.530
Felleisen RSJ (1997) Comparative sequence analysis of 5.8S rRNA genes and internal transcribed spacer (ITS) regions of trichomonadid protozoa. Parasitology 115:111–119
Filho GAPC, Oliveira JMB, Andrade MR, Silva JG, Kim PC, Almeida JC, Porto WJM, Mota RA (2017) Incidence and vertical transmission rate of Neospora caninum in sheep. Comp Immunol Microbiol Infect 52:19–22. https://doi.org/10.1016/j.cimid.2017.05.006
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. https://doi.org/10.1017/S0031182017000646
Holsback L, Lima HE, Vidotto O, Silva MA, Patelli TH, Martins FD, Seixas MD (2018) Cryptosporidium occurrence in ruminants from the North Pioneer mesoregion of Paraná, Brazil. Rev Bras Parasitol Vet 27:248–253. https://doi.org/10.1590/s1984-296120180037
Honigberg BM (1963) Evolutionary and systematic relationships in the flagellate order Trichomonadida Kirby. J Protozool 10:20–63
Ibañez-Escribano A, Nogal-Ruiz JJ, Delclaux M, Martinez-Nevado E, Ponce-Gordo F (2013) Morphological and molecular identification of Tetratrichomonas flagellates from the giant anteater (Myrmecophaga tridactyla). Res Vet Sci 95:176–181. https://doi.org/10.1016/j.rvsc.2013.01.022
Instituto Brasileiro de Geografia e Estatística – IBGE (2017) Censo agropecuário. Publishing PhysicsWeb https://censos.ibge.gov.br/agro/2017/. Accessed 25 May 2017
Jensen EA, Hammond DM (1964) A morphological study of trichomonads and related flagellates from the bovine digestive tract. J Protozool 11:386–394. https://doi.org/10.1111/j.1550-7408.1964.tb01768.x
Jesus JB, Vannier-Santos MA, Britto C, Godefroy P, Silva-Filho FC, Pinheiro AA, Rocha-Azevedo B, Lopes AH, Meyer-Fernandes JR (2004) Trichomonas vaginalis virulence against epithelial cells and morphological variability: the comparison between a well-established strain and a fresh isolate. Parasitol Res 93:369–377. https://doi.org/10.1007/s00436-004-1134-4
Kellerová P, Tachezy J (2017) Zoonotic Trichomonas tenax and a new trichomonad species, Trichomonas brixi n. sp., from the oral cavities of dogs and cats. Int J Parasitol 47:247–255. https://doi.org/10.1016/j.ijpara.2016.12.006
Kleina P, Bettim-Bandinelli J, Bonatto SL, Benchimol M, Bogo MR (2004) Molecular phylogeny of Trichomonadidae family inferred from ITS-1, 5.8 S rRNA and ITS-2 sequences. Int J Parasitol 34:963–970. https://doi.org/10.1016/j.ijpara.2004.04.004
Kofer J, Hofer H, Hartmann S (2017) Next-generation parasitologists: structured training programs meet educational challenges. Trends Parasitol 33:423–425. https://doi.org/10.1016/j.pt.2017.03.008
Landman WJM, Molenaar RJ, Cian A, Van Der Heijden HMJF, Viscogliosi E (2016) Granuloma disease in flocks of productive layers caused by Tetratrichomonas gallinarum. Avian Pathol 45:465–477. https://doi.org/10.1080/03079457.2016.1163325
Learmount J, Taylor MA, Smith G, Morgan C (2006) A computer model to simulate control of parasitic gastroenteritis in sheep on UK farms. Vet Parasitol 142:312–329. https://doi.org/10.1016/j.vetpar.2006.07.012
Li WC, Wang K, Gu Y (2018) Occurrence of Blastocystis sp. and Pentatrichomonas hominis in sheep and goats in China. Parasit Vectors 11:93–100. https://doi.org/10.1186/s13071-018-2671-5
Lopez-Escamilla E, Sanchez-Aguillon F, Alatorre-Fernandez CP, Aguilar-Zapata D, Arroyo-Escalante S, Arellano T, Moncada-Barron D, Romero-Valdovinos M, Martinez-Hernandez F, Rodriguez-Zulueta P, Maravilla P (2013) New Tetratrichomonas species in two patients with pleural empyema. J Clin Microbial 51:3143–3146. https://doi.org/10.1128/JCM.01056-13
Lun ZR, Gajadhar AA (1999) A simple and rapid method for staining Tritrichomonas foetus and Trichomonas vaginalis. J Vet Diagn Investig 11:471–474
Magalhães FJR, Ribeiro-Andrade M, Alcântara AMD, Pinheiro Júnior JW, Sena MJD, Porto WJN, Vieira RFC, Mota RA (2016) Risk factors for Toxoplasma gondii infection in sheep and cattle from Fernando de Noronha Island, Brazil. Rev Bras Parasitol Vet 25:511–515. https://doi.org/10.1590/s1984-29612016051
Maritz JM, Land KM, Carlton JM (2014) Hirt RP (2014) What is the importance of zoonotic trichomonads for human health? Trends Parasitol 30:333–341. https://doi.org/10.1016/j.pt.2014.05.005
Meggiolaro MN, Roeber F, Kobylski V, Higgins DP, Šlapeta J (2019) Comparison of multiplexed-tandem real-time PCR panel with reference real-time PCR molecular diagnostic assays for detection of Giardia intestinalis and Tritrichomonas foetus in cats. Vet Parasitol 266:12–17. https://doi.org/10.1016/j.vetpar.2018.12.009
Nadler SA, de León GP (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138:1688–1709. https://doi.org/10.1017/S003118201000168X
Nelson EC (1940) An intestinal content cultivation medium. Am J Trop Med Hyg 1:731–745
Ondrak JD (2016) Tritrichomonas foetus prevention and control in cattle. Vet Clin Food Anim Pract 32:411–423. https://doi.org/10.1016/j.cvfa.2016.01.010
Paes e Silva M, Lopes R, Bresciani K, Amarante A, Araujo J (2014) High occurrence of Cryptosporidium ubiquitum and Giardia duodenalis genotype E in sheep from Brazil. Acta Parasitol 59:193–196. https://doi.org/10.2478/s11686-014-0223-5
Ribeiro ELA, González-García E (2016) Indigenous sheep breeds in Brazil: potential role for contributing to the sustainability of production systems. Trop Anim Health Prod 48:1305–1313. https://doi.org/10.1007/s11250-016-1109-3
Ribeiro LC, Santos C, Benchimol M (2015) Is Trichomonas tenax a parasite or a commensal? Protist 166:196–210. https://doi.org/10.1016/j.protis.2015.02.002
Riedmüller, L (1928) Über die morphologie, überträgungsversuche, und klinischebedeutung der beimsporadischen abortus des rindesvorkommenden Trichomonaden. Zentralblatt Fur Bakteriologie Parasitenkunde Infektionskranheiten und Hygiene Abteilung 1-Originale Medizinisch Hygiensche Bakteriologie Virusforschung und Parasitologie 108:103–118
Rivera WL, Lupisan AJB, Baking JMP (2008) Ultrastructural study of a tetratrichomonad isolated from pig fecal samples. Parasitol Res 103:1311–1316. https://doi.org/10.1007/s00436-008-1134-x
Robertson A (1932) Note on a Trichomonas sp. cultivated from the gut of a sheep Ditrichomonas ovis. Vet J 88:151–157
Rose H, Wang T, Van Dijk J, Morgan ER (2015) GLOWORM-FL: a simulation model of the effects of climate and climate change on the free-living stages of gastro-intestinal nematode parasites of ruminants. Ecol Model 297:232–245. https://doi.org/10.1016/j.ecolmodel.2014.11.033
Schwebke JR, Burgess D (2004) Trichomoniasis. Clin Microbial Rev 17:794–803. https://doi.org/10.1128/CMR.17.4.794-803.2004
Smejkalová P, Petrželková KJ, Pomajbíková K, Modrý D, Cépicka I (2011) Extensive diversity of intestinal trichomonads of non-human primates. Parasitology 139:92–102. https://doi.org/10.1017/S0031182011001624
Snak A, Smiderle FR, Mello Fernandes NL, Lara AA, Garcia FG, Ogawa L, Osaki SC (2017) Occurrence and molecular characterization of Cryptosporidium sp. in sheep. Semina: Ciênc Agrár 38:1917–1924. https://doi.org/10.5433/1679-0359.2017v38n4p1917
Taylor M (2000) Protozoal disease in cattle and sheep. Pract Lond Br Vet Assoc 22:604–626
Verweij JJ, Van Belkum A, Stensvold CR (2016) Molecular detection of gastrointestinal parasites. Mol Microbiol:530–541
Walker RL, Hayes DC, Sawyer SJ, Nordhausen RW, Van Hoosear KA, Bondurant RH (2003) Comparison of the 5.8 S rRNA gene and internal transcribed spacer regions of trichomonadid protozoa recovered from the bovine preputial cavity. J Vet Diagn Investig 15:14–20. https://doi.org/10.1177/104063870301500104
Yao C, Köster LS (2015) Tritrichomonas foetus infection, a cause of chronic diarrhea in the domestic cat. Vet Res 46:35. https://doi.org/10.1186/s13567-015-0169-0
Acknowledgments
The authors would like to acknowledge the generosity of the farm owners for providing access to their animals and informed consent for fecal sampling, especially to veterinarian Daniel Marchesi Neves. We also thank undergraduate student Cezar Augusto da Silva and Professor Carlos Wilson Gomes Lopes (UFRRJ) for their attention and assistance in preparing this manuscript.
Funding
The research reported in this article was financially supported in part by funding from the National Council for Scientific and Technological Development (CNPq).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All aspects of the study involving animals were conducted in strict accordance with the recommendations established by the Ethics committee of the Federal Rural University of Rio de Janeiro Federal Rural, under the conditions outlined in the license (CEUA/IV/UFRRJ no. 2614120717). We declare that the animals were not harmed in any way during the experimental procedures.
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
Carreiro, C.C., McIntosh, D., dos Santos, D.J. et al. Morphological and molecular characterization of a species of Tetratrichomonas present in feces of Brazilian sheep (Ovis aries) and goats (Capra hircus). Parasitol Res 119, 233–242 (2020). https://doi.org/10.1007/s00436-019-06466-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06466-9