We investigated intestinal trichomonads in western lowland gorillas, central chimpanzees and humans cohabiting the forest ecosystem of Dzanga-Sangha Protected Area in Central African Republic, using the internal transcribed spacer (ITS) region and SSU rRNA gene sequences. Trichomonads belonging to the genus Tetratrichomonas were detected in 23% of the faecal samples and in all host species. Different hosts were infected with different genotypes of Tetratrichomonas. In chimpanzees, we detected tetratrichomonads from 'novel lineage 2', which was previously reported mostly in captive and wild chimpanzees. In gorillas, we found two different genotypes of Tetratrichomonas. The ITS region sequences of the more frequent genotype were identical to the sequence found in a faecal sample of a wild western lowland gorilla from Cameroon. Sequences of the second genotype from gorillas were almost identical to sequences previously obtained from an anorexic French woman. We provide the first report of the presence of intestinal tetratrichomonads in asymptomatic, apparently healthy humans. Human tetratrichomonads belonged to the lineage 7, which was previously reported in domestic and wild pigs and a domestic horse. Our findings suggest that the ecology and spatial overlap among hominids in the tropical forest ecosystem has not resulted in exchange of intestinal trichomonads among these hosts.

Departamento de Ecología y Biodiversidad Facultad de Ciencias de la Vida Universidad Andrés Bello Republica 440 Santiago Chile

Department of Medical Biology Faculty of Sciences University of South Bohemia Branišovská 31 České Budějovice 370 05 Czech Republic

Department of Parasitology Faculty of Science Charles University Viničná 7 128 44Prague Czech Republic

Department of Pathology and Parasitology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Palackého tř 1946 1 612 42Brno Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 128 44Prague Czech Republic

Dzanga Sangha Project World Wildlife Fund Bangui Central African Republic

European Institute for Technology University of Veterinary and Pharmaceutical Sciences Brno Palackého tř 1946 1 612 42Brno Czech Republic

Fauna and Flora International Pembroke St Cambridge CB2 3QZ UK

Liberec Zoo Lidové sady 425 1 460 01Liberec Czech Republic

The Czech Academy of Sciences Biology Centre Institute of Parasitology Branišovská 31 370 05České Budějovice Czech Republic

The Czech Academy of Sciences Institute of Vertebrate Biology Květná 8 603 65Brno Czech Republic

Zobrazit více v PubMed

Blom A, Almasi A, Heitkonig IMA, Kpanou JB and Prins HHT (2001) A survey of the apes in the Dzanga-Ndoki National Park, Central African Republic: a comparison between the census and survey methods of estimating the gorilla (Gorilla gorilla gorilla) and chimpanzee (Pan troglodytes) nest group density. African Journal of Ecology 39, 98–105.

Calvignac-Spencer S, Leendertz SAJ and Gillespie TR (2012) Wild great apes as sentinels and sources of infectious disease. Clinical Microbiology and Infection 18, 521–527. PubMed

Carroll RW (1986) The Creation, Development, Protection, and Management of the Dzanga-Sangha Dense Forest Sanctuary and the Dzanga-Ndoki National Park in Southwestern Central African Republic. New Haven, Connecticut: Yale University School of Forestry and Environmental Studies.

Cepicka I, Kutisová K, Tachezy J, Kulda J and Flegr J (2005) Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology 128, 11–21. PubMed

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, 542–551. PubMed

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, 400–433. PubMed

Čepička I, Dolan MF and Gile GH (2017) Parabasalia. In Archibald JM, Simpson AGB and Slamovits CH (eds), Handbook of the Protists. Cham, Switzerland: Springer, pp. 1175–1218.

Chabé M, Lokmer A and Ségurel L (2017) Gut protozoa: friends or foes of the human gut microbiota? Trends in Parasitology 33, 925–934. PubMed

Clayton JB, Vangay P, Huang H, Ward T, Hillmann BM, Al-Ghalith GA, Travis DA, Long HT, Tuan BV, Minh VV, Cabana F, Nadler T, Toddes B, Murphy T, Glander KE, Johnson TJ and Knights D (2016) Captivity humanizes the primate microbiome. Proceedings of the National Academy of Sciences 113, 10376–10381. PubMed PMC

Dobell C and Laidlaw PP (1926) On the cultivation of Entamoeba histolytica and some other entozoic amoebae. Parasitology 18, 283–318.

dos Santos CS, de Jesus VLT, McIntosh D, Carreiro CC, Batista LCO, do Bomfim Lopez B, Neves DM and Lopes CWG (2017) Morphological, ultrastructural, and molecular characterization of intestinal tetratrichomonads isolated from non-human primates in southeastern Brazil. Parasitology Research 116, 2479–2488. PubMed

Flick EW (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, 105–121. PubMed

Gomez A, Petrzelkova K, Yeoman CJ, Vlckova K, Mrázek J, Koppova I, Carbonero F, Ulanov A, Modry D, Todd A, Torralba M, Nelson KE, Gaskins HR, Wilson B, Stumpf RM, White BA and Leigh S (2015) Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Molecular Ecology 24, 2551–2565. PubMed

Gouba N, Raoult D and Drancourt M (2014) Gut microeukaryotes during anorexia nervosa: a case report. BMC Research Notes 7, 33–36. PubMed PMC

Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.

Hamad I, Keita MB, Peeters M, Delaporte E, Raoult D and Bittar F (2014) Pathogenic eukaryotes in gut microbiota of western lowland gorillas as revealed by molecular survey. Scientific Reports 4, 6417. PubMed PMC

Hasegawa H, Modrý D, Kitagawa M, Shutt KA, Todd A, Kalousová B, Profousova I and Petrželková KJ (2014) Great apes cohabiting the forest ecosystem in Central African Republic harbour the same hookworms. PLoS Neglected Tropical Diseases 8, e2715. PubMed PMC

Honigberg BM (1978) Trichomonads of veterinary importance. In Kreier JP (ed.), Parasitic Protozoa, vol. 2. New York, US: Academic Press, pp. 163–273.

Honigberg BM (1990) Trichomonads Parasitic in Humans. New York, US: Springer.

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, 3059–3066. PubMed PMC

Ibañez-Escribano A, Nogal-Ruiz JJ, Delclaux M, Martinez-Nevado E and Ponce-Gordo F (2013) Morphological and molecular identification of Tetratrichomonas flagellates from the giant anteater (Myrmecophaga tridactyla). Research in Veterinary Science 95, 176–181. PubMed

Keane TM, Creevey CJ, Pentony MM, Naughton TJ and McInerney JO (2004) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology 6, 29. PubMed PMC

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, 309–319. PubMed

Li WC, Ying M, Gong PT, Li JH, Yang J, Li H and Zhang XC (2016) Pentatrichomonas hominis: prevalence and molecular characterization in humans, dogs, and monkeys in Northern China. Parasitology Research 115, 569–574. PubMed

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 and Maravilla P (2013) New Tetratrichomonas species in two patients with pleural empyema. Journal of Clinical Microbiology 51, 3143–3146. PubMed PMC

Maritz JM, Land KM, Carlton JM and Hirt RP (2014) What is the importance of zoonotic trichomonads for human health? Trends in Parasitology 30, 333–341. PubMed PMC

Myers BJ and Kuntz RE (1972) A checklist of parasites and commensals reported for the chimpanzee (Pan). Primates 13, 433–471. PubMed

Pafčo B, Benavides JA, Pšenková-Profousová I, Modrý D, Červená B, Shutt KA, Hasegawa H, Fuh T, Todd AF and Petrželková KJ (2017) Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas? Parasitology Research 116, 3401–3410. PubMed

Pafčo B, Čížková D, Kreisinger J, Hasegawa H, Vallo P, Shutt K, Todd A, Petrželková KJ and Modrý D (2018) Metabarcoding analysis of strongylid nematode diversity in two sympatric primate species. Scientific Reports 8, 5933. PubMed PMC

Ratcliffe LH (1928) The numbers of trichomonads in rats on diets of different protein content in relation to pH and bacteria in the cecum. American Journal of Epidemiology 8, 910–934.

Reardon LV and Rininger BF (1968) A survey of parasites in laboratory primates. Laboratory Animal Care 18, 577–580. PubMed

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA and Huelsenbeck JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542. PubMed PMC

Rowan-Nash AD, Korry BJ, Mylonakis E and Belenky P (2019) Cross-domain and viral interactions in the microbiome. Microbiology and Molecular Biology Reviews 83, e00044. PubMed PMC

Rushmore J, Allison AB, Edwards EE, Bagal U, Altizer S, Cranfield MR, Glenn TC, Liu H, Mudakikwa A, Mugisha L, Muller MN, Stumpf RM, Thompson ME, Wrangham R and Yabsley MJ (2015) Screening wild and semi-free ranging great apes for putative sexually transmitted diseases: evidence of Trichomonadidae infections. American Journal of Primatology 77, 1075–1085. PubMed

Sak B, Petrzelkova KJ, Kvetonova D, Mynarova A, Shutt KA, Pomajbikova K, Kalousova B, Modry D, Benavides J, Todd A and Kvac M (2013) Long-term monitoring of microsporidia, Cryptosporidium and Giardia infections in western lowland gorillas (Gorilla gorilla gorilla) at different stages of habituation in Dzanga Sangha Protected Areas, Central African Republic. PLoS One 8, e71840. PubMed PMC

Smejkalová P, Petrželková KJ, Pomajbíková K, Modrý D and Čepička I (2012) Extensive diversity of intestinal trichomonads of non-human primates. Parasitology 139, 92–102. PubMed

Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 1312–1313. PubMed PMC

Tachezy J, Tachezy R, Hampl V, Sedinova M, Vanacova S, Vrlik M, van Ranst M, Flegr J and Kulda J (2002) Cattle pathogen Tritrichomonas foetus (Riedmuller, 1928) and pig commensal Tritrichomonas suis (Gruby & Delafond, 1843) belong to the same species. Journal of Eukaryotic Microbiology 49, 154–163. PubMed

Tai V, James ER, Nalepa CA, Scheffrahn RH, Perlman SJ and Keeling CJ (2015) The role of host phylogeny varies in shaping microbial diversity in the hindguts of lower termites. Applied and Environmental Microbiology 81, 1059–1070. PubMed PMC

Walker RL, Hayes DC, Sawyer RW, Nordhausen RW, Van Hoosear KA and BonDurant RH (2003) Comparison of the 5.8S rRNA gene and internal transcribed spacer regions of trichomonadid protozoa recovered from the bovine preputial cavity. Journal of Veterinary Diagnostic Investigation 15, 14–20. PubMed

Wenrich DH (1944) Morphology of the intestinal trichomonad flagellates in man and of similar forms in monkeys, cats, dogs and rats. Journal of Morphology 74, 189–211.

Wong ZW, Faulder K and Robinson JL (2018) Does Dientamoeba fragilis cause diarrhea? A systematic review. Parasitology Research 117, 971–980. PubMed