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Extensive diversity of intestinal trichomonads of non-human primates

Published online by Cambridge University Press:  26 September 2011

PAVLA SMEJKALOVÁ
Affiliation:
Department of Parasitology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44 Prague, Czech Republic Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44, Prague, Czech Republic
KLÁRA J. PETRŽELKOVÁ
Affiliation:
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Květná 8, 603 65 Brno, Czech Republic Liberec ZOO, Masarykova 1347/31, 460 01 Liberec, Czech Republic
KATEŘINA POMAJBÍKOVÁ
Affiliation:
Department of Parasitology, University of Veterinary and Pharmaceutical Sciences, Palackého 1-3, 612 42 Brno, Czech Republic
DAVID MODRÝ
Affiliation:
Department of Parasitology, University of Veterinary and Pharmaceutical Sciences, Palackého 1-3, 612 42 Brno, Czech Republic Biology Center, Institute of Parasitology, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic
IVAN ČEPIČKA*
Affiliation:
Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44, Prague, Czech Republic
*
*Corresponding author: Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44, Prague, Czech Republic. Tel: +420 221951842. Fax: +420 221951841. E-mail: [email protected]

Summary

Despite the fact that the non-human primates are our closest relatives and represent a species-rich mammalian group, little is known about their intestinal protistan parasites/commensals. Particularly, the intestinal trichomonads represent a neglected part of the fauna of the primate digestive system. We have established 30 trichomonad strains isolated from feces of 11 primate species kept in 3 Czech zoos and performed an analysis of their SSU rDNA and ITS1-5·8S rDNA-ITS2. Our results showed that intestinal trichomonads are rather common among non-human primates. Molecular phylogenetic analysis showed that the strains are unexpectedly diversified, belonging to 8 or 9 distinct species. Interestingly, the vast majority of the strains from non-human primates belonged to the genus Tetratrichomonas while no member of this genus has been found in the human intestine so far. In addition, hominoid and non-hominoid primates differed in their intestinal trichomonads. Our results suggest that captive primates possibly may be infected by intestinal trichomonads of other vertebrates such as pigs, cattle, birds, tortoises and lizards.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Abraham, R. (1961). The morphology of Monocercomonas lori n. sp., from the Indian slender loris. Archiv für Protistenkunde 105, 445449.Google Scholar
Abraham, R. (1962). A new species of Trichomonas (Protozoa: Mastigophora) parasitic in slender loris. Zeitschrift für Parasitenkunde 21, 202206.CrossRefGoogle ScholarPubMed
Adl, S. M., Leander, B. S., Simpson, A. G. B., Archibald, J. M., Anderson, O. R., Bass, D., Bowser, S. S., Brugerolle, G., Farmer, M. A., Karpov, S., Kolisko, M., Lane, C. E., Lodge, D. J., Mann, D. G., Meisterfeld, R., Mendoza, L., Moestrup, Ø., Mozley-Standridge, S. E., Smirnov, A. V. and Spiegel, F. (2007). Diversity, nomenclature, and taxonomy of protists. Systematic Biology 56, 684689. doi: 10.1080/10635150701494127.CrossRefGoogle ScholarPubMed
Carmody, R. N. and Wrangham, R. W. (2009). The energetic significance of cooking. Journal of Human Evolution 57, 379391. doi: 10.1016/j.jhevol.2009.02.011.CrossRefGoogle ScholarPubMed
Carmona, M. C., Bermudez, O. G., Gutierrez-Espeleta, G. A., Porras, R. S. and Ortiz, B. R. (2005). Intestinal parasites in howler monkeys Alouatta palliata (Primates: Cebidae) of Costa Rica. Revista de Biologia Tropical 53, 437445.CrossRefGoogle ScholarPubMed
Cavalier-Smith, T. (2002). The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. International Journal of Systematic and Evolutionary Microbiology 52, 297354. doi: 10.1099/ijs.0.02058-0.CrossRefGoogle ScholarPubMed
Cepicka, I., Hampl, V. and Kulda, J. (2010). Critical taxonomic revision of parabasalids with description of one new genus and three new species. Protist 161, 400433. doi: 10.1016/j.protis.2009.11.005.CrossRefGoogle ScholarPubMed
Cepicka, I., Hampl, V., Kulda, J. and Flegr, J. (2006). New evolutionary lineages, unexpected diversity, and host specificity in the parabasalid genus Tetratrichomonas. Molecular Phylogenetics and Evolution 39, 542551. doi:10.1016/j.ympev.2006.01.005.CrossRefGoogle ScholarPubMed
Cepicka, I., Kutišová, K., Tachezy, J., Kulda, J. and Flegr, J. (2005). Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology 128, 1121. doi:10.1016/j.vetpar.2004.11.003.CrossRefGoogle ScholarPubMed
Cleveland, L. R. (1928). Tritrichomonas fecalis nov. sp. of man; its ability to grow and multiply indefinitely in faeces with tap water and in frogs and tadpoles. American Journal of Hygiene 8, 232255.Google Scholar
Culbertson, D. E., Pindak, F. F., Gardner, W. A. and Honigberg, B. M. (1986). Tritrichomonas mobilensis n. sp. (Zoomastigophorea: Trichomonadida) from the Bolivian squirrel monkey Saimiri boliviensis boliviensis. Journal of Protozoology 33, 301304.CrossRefGoogle Scholar
Cutillas, C., Callejon, R., de Rojas, M., Tewes, B., Ubeda, J. M., Ariza, C. and Guevara, D. C. (2009). Trichuris suis and Trichuris trichiura are different nematode species. Acta Tropica 111, 299307. doi:10.1016/j.actatropica.2009.05.011.CrossRefGoogle ScholarPubMed
Deschiens, R. (1927). Sur les protozoaires intestinaux des singes. Bulletin of the Exotic Pathology Society 20, 1923.Google Scholar
Dobell, C. and Leidlaw, P. P. (1926). On the cultivation of Entamoeba histolytica and some other entozoic amoebae. Parasitology 18, 283318.CrossRefGoogle Scholar
Duboucher, C., Caby, S., Dufernez, F., Chabé, M., Gantois, N., Delgado-Viscogliosi, P., Billy, C., Barré, E., Torabi, E., Capron, M., Pierce, R. J., Dei-Cas, E. and Viscolgiosi, E. (2006). Molecular identification of Tritrichomonas foetus-like organisms as coinfecting agents of human Pneumocystis pneumonia. Journal of Clinical Microbiology 44, 11651168. doi:10.1128/JCM.44.3.1165-1168.2006.CrossRefGoogle ScholarPubMed
Dufernez, F., Walker, R. L., Noël, C., Caby, S., Mantini, C., Delgado-Viscogliosi, P., Ohkuma, M., Kudo, T., Capron, M., Pierce, R. J., Villanueva, M. R. and Viscogliosi, E. (2007). Morphological and molecular identification of non-Tritrichomonas foetus trichomonad protozoa from the bovine preputial cavity. Journal of Eukaryotic Microbiology 54, 161168. doi: 10.1111/j.1550-7408.2007.00247.x.CrossRefGoogle ScholarPubMed
Flick, E. W. (1954). Experimental analysis of some factors influencing variation in the flagellar number of Trichomonas hominis from man and other primates and their relationship to nomenclature. Experimental Parasitology 3, 105121.CrossRefGoogle ScholarPubMed
Greiner, E. C. and McIntosh, A. (2009). Collection methods and diagnostic procedures for primate parasitology. In Primate Parasite Ecology (ed. Huffman, M. A. and Chapman, C.), pp. 327. Cambridge University Press, Cambridge, UK.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704. doi: 10.1080/10635150390235520.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hampl, V., Cepicka, I., Flegr, J., Tachezy, J. and Kulda, J. (2007). Morphological diversity of the monocercomonadid genera Monocercomonas, Hexamastix, and Honigbergiella gen. nov. Protist 158, 365383. doi: 10.1016/j.protis.2007.02.003.CrossRefGoogle ScholarPubMed
Hasegawa, H., Sato, H., Fujita, S., Nguema, P. P. M., Nobusue, K., Miyagi, K., Kooriyama, T., Takenoshita, Y., Noda, S., Sato, A, Morimoto, A., Ikeda, Y. and Nishida, T. (2010). Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania: Dispersal and diversity of Strongyloides spp. and their hosts. Parasitology International 59, 407413. doi: 10.1016/j.parint.2010.05.007.CrossRefGoogle ScholarPubMed
Hegner, R. and Ratcliffe, H. (1927). Trichomonads from the vagina of the monkey, from the mouth of the cat and man, and from the intestine of the monkey, opossum and prairie-dog. Journal of Parasitology 14, 2735.CrossRefGoogle Scholar
Honigberg, B. M. (1978 a). Trichomonads of veterinary importance. In Parasitic Protozoa II (ed. Kreier, J. P.), pp. 163273. Academic Press, New York, USA.Google Scholar
Honigberg, B. M. (1978 b). Trichomonads of importance in human medicine. In Parasitic Protozoa II (ed. Kreier, J. P.), pp. 275454. Academic Press, New York, USA.Google Scholar
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi: 10.1093/bioinformatics/17.8.754.CrossRefGoogle ScholarPubMed
Johnston, A. R., Gillespie, T. R., Rwego, I. B., McLachlan, T. L. T., Kent, A. D. and Goldberg, T. L. (2010). Molecular epidemiology of cross-Species Giardia duodenalis transmission in Western Uganda. PLOS Neglected Tropical Diseases 4: e683. doi: 10.1371/journal.pntd.0000683.CrossRefGoogle ScholarPubMed
Katoh, K., Misawa, K., Kuma, K. and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 30593066. doi: 10.1093/nar/gkf436.CrossRefGoogle ScholarPubMed
Krief, S., Vermeulen, B., Lafosse, S., Kasenene, J. M., Nieguitsila, A., Berthelemy, M., L'Hostis, M., Bain, O. and Guillot, J. (2010). Nodular worm infection in wild chimpanzees in Western Uganda: A risk for human health? PLOS Neglected Tropical Diseases 4, e630. doi: 10.1371/journal.pntd.0000630.CrossRefGoogle ScholarPubMed
Kutisova, K., Kulda, J., Cepicka, I., Flegr, J., Koudela, B., Teras, J. and Tachezy, J. (2005). Tetratrichomonads from the oral cavity and respiratory tract of humans. Parasitology 131, 309319. doi: 10.1017/S0031182005008000.CrossRefGoogle ScholarPubMed
Lankester, F., Kiyang, J. A., Bailey, W., Unwin, S. (2010). Dientamoeba fragilis: initial evidence of pathogenicity in the western lowland gorilla (Gorilla gorilla gorilla). Journal of Zoo and Wildlife Medicine 41, 350352. doi: 10.1638/2009-0190.1.CrossRefGoogle ScholarPubMed
Levecke, B., Geldhof, P., Claerebout, E., Dorny, P., Vercammen, F., Cacciò, S. M., Vercuysse, J. and Geurden, T. (2009). Molecular characterisation of Giardia duodenalis in captive non-human primates reveals mixed assemblage A and B infections and novel polymorphisms. International Journal for Parasitology 39, 15951601. doi: 10.1016/j.ijpara.2009.05.013CrossRefGoogle Scholar
Levy, M. G., Gookin, J. L., Poore, M., Birkenheuer, A. J., Dykstra, M. J. and Litaker, R. W. (2003). Tritrichomonas foetus and not Pentatrichomonas hominis is the etiological agent of the feline trichomonal diarrhea. Journal of Parasitology 89, 99104.CrossRefGoogle Scholar
Lilly, A. A., Mehlman, P. T. and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and human at Mondika research site, Dzanga-Ndoki national park, Central African Republic. International Journal of Primatology 23, 555573.CrossRefGoogle Scholar
Mantini, C., Souppart, L., Noël, C., Duong, T. H., Mornet, M., Carroger, G., Dupont, P., Masseret, E., Goustille, J., Capron, M., Duboucher, C., Dei-Cas, E. and Viscogliosi, E. (2009). Molecular characterization of a new Tetratrichomonas species in a patient with empyema. Journal of Clinical Microbiology 47, 22362339. doi: 10.1128/JCM.00353-09.CrossRefGoogle Scholar
McDougald, L. R. and Reid, W. M. (1978). Histomonas meleagridis and relatives. In Parasitic Protozoa II (ed. Kreier, J. P.), pp. 139161. Academic Press, New York, USA.Google Scholar
Myers, B. J. and Kuntz, R. E. (1972). A checklist of parasites and commensals reported for the chimpanzee (Pan). Primates 13, 433471.CrossRefGoogle ScholarPubMed
Parkar, U., Traub, R. J., Vitali, S., Vitali, S., Elliot, A., Levecke, B., Robertson, I., Geurden, T., Steele, J., Drake, B. and Thompson, R. C. A. (2010). Molecular characterization of Blastocystis isolates from zoo animals and their animal-keepers. Veterinary Parasitology 169, 817. doi: 10.1016/j.vetpar.2009.12.032.CrossRefGoogle ScholarPubMed
Pindak, F. F. and de Pindak, M. M. (1998). Diagnostic characteristics of owl monkey (Aotus trivirgatus) intestinal trichomonads. Acta Protozoologica 37, 159172.Google Scholar
Pomajbíková, K., Petrželková, K. J., Profousová, I., Petrašová, J., Kišidayová, S., Varadyová, Z. and Modrý, D. (2010). A survey of entodiniomorphid ciliates in chimpanzees and bonobos. American Journal of Physical Anthropology 42, 4248. DOI: 10.1002/ajpa.21191.CrossRefGoogle Scholar
Posada, D. and Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817818.CrossRefGoogle ScholarPubMed
Prugnolle, F., Duran, P., Neel, C., Ollomo, B., Ayala, F. J., Arnathau, C., Etienne, L., Mpondi-Ngole, E., Nkoghe, D., Leroy, E., Delaporte, E., Peeters, M. and Renaud, F. (2009). African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 107, 14581463. doi: 10.1073/pnas.0914440107.CrossRefGoogle Scholar
Ratcliffe, H. L. (1928). The numbers of trichomonads in rats on diets of different protein content in relation to the pH and bacteria in the cecum. Americal Journal of Epidemiology 8, 910934.CrossRefGoogle Scholar
Reardon, L. V. and Rininger, B. F. (1968). A survey of parasites in laboratory primates. Laboratory Animal Care 18, 577580.Google ScholarPubMed
Stahl, A. B, Dunbar, R. I. M., Homewood, K., Ikawa-Smith, F., Kortlandt, A., McGrew, W. C., Milton, K., Paterson, D. J., Poirier, F. E., Sugardjito, J., Tanner, N. M. and Wrangham, R. W. (1984). Hominid dietary selection before fire [and Comments and Reply]. Current Anthropology 25, 151168.CrossRefGoogle Scholar
Stark, D., Phillips, O., Peckett, D., Munro, U., Marriott, D., Harkness, J. and Ellis, J. (2008). Gorillas are a host for Dientamoeba fragilis: an update on the life cycle and host distribution. Veterinary Parasitology 151, 2126. doi: 10.1016/j.vetpar.2007.10.002.CrossRefGoogle ScholarPubMed
Stensvold, C. R., Alfellani, M. A., Nørskov-Lauritsen, S., Prip, K., Victory, E. L., Maddox, C., Nielsen, H. V. and Clark, C. G. (2009). Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. International Journal for Parasitology 39, 473479. doi: 10.1016/j.ijpara.2008.07.006.CrossRefGoogle ScholarPubMed
Suzuki, J., Kobayashi, S., Murata, R., Tajima, H., Hashizaki, F., Yanagawa, Y. and Takeuchi, T. (2008). A survey of amoebic infections and differentiation of an Entamoeba histolytica-like variant (JSK2004) in nonhuman primates by a multiplex polymerase chain reaction. Journal of Zoo and Wildlife Medicine 39, 370379. doi: 10.1638/2007-0171.1.CrossRefGoogle ScholarPubMed
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4.0b10. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Tachezy, J., Tachezy, R., Hampl, V., Šedinová, M., Vaňáčová, Š., Vrlík, M., Van Ranst, M., Flegr, J. and Kulda, J. (2002). Cattle pathogen Tritrichomonas foetus (Riedmüller, 1928) and pig commensal Tritrichomonas suis (Gruby & Delafond, 1843) belong to the same species. Journal of Eukaryotic Microbiology 49, 154163. doi: 10.1111/j.1550-7408.2002.tb00360.x.CrossRefGoogle Scholar
Tachibana, H., Yanagi, T., Akatsuka, A., Kobayash, S., Kanbara, H. and Tsutsumi, V. (2009). Isolation and characterization of a potentially virulent species Entamoeba nuttalli from captive Japanese macaques. Parasitology 136, 11691177. doi: 10.1017/S0031182009990576.CrossRefGoogle ScholarPubMed
Tokiwa, T., Modrý, D., Ito, A., Pomajbíková, K., Petrželková, K. J. and Imai, S. (2010). A new entodiniomorphid ciliate, Troglocorys cava n. g., n. sp., from the wild Eastern chimpanzee. Journal of Eukaryotic Microbiology 57, 115120. DOI: 10.1111/j.1550-7408.2009.00456.x.CrossRefGoogle Scholar
Wenrich, D. H. (1944 a). Morphology of the intestinal trichomonad flagellates in man and of similar forms in monkeys, cats, dogs and rats. Journal of Morphology 74, 189211.CrossRefGoogle Scholar
Wenrich, D. H. (1944 b). Comparative morphology of the trichomonad flagellates of man. American Journal of Tropical Medicine and Hygiene 24, 3951.CrossRefGoogle Scholar
Wenrich, D. H. and Nie, D. (1949). The morphology of Trichomonas wenyoni (Protozoa, Mastigophora). Journal of Morphology 85, 519531.CrossRefGoogle ScholarPubMed
Wrangham, R. and Conklin-Brittain, N. L. (2003). ‘Cooking as a biological trait.’. Comparative Biochemistry and Physiology Part A 136, 3546. doi: 10.1016/S1095-6433(03)00020-5.CrossRefGoogle ScholarPubMed
Yubuki., N., Céza, V., Cepicka, I., Yabuki, A., Inagaki, Y., Nakayama, T., Ionuye, I. and leander, B. S. (2010). Cryptic diversity of free-living parabasalids, Pseudotrichomonas keilini and Lacusteria cypriaca n. gen., n. sp., as inferred from small subunit rDNA sequences. Journal of Eukaryotic Microbiology 57, 554561. doi: 10.1111/j.1550-7408.2010.00509.x.CrossRefGoogle Scholar