Balantidiasis is considered a neglected zoonotic disease with pigs serving as reservoir hosts. However, Balantidium coli has been recorded in many other mammalian species, including primates. Here, we evaluated the genetic diversity of B. coli in non-human primates using two gene markers (SSrDNA and ITS1-5.8SDNA-ITS2). We analyzed 49 isolates of ciliates from fecal samples originating from 11 species of captive and wild primates, domestic pigs and wild boar. The phylogenetic trees were computed using Bayesian inference and Maximum likelihood. Balantidium entozoon from edible frog and Buxtonella sulcata from cattle were included in the analyses as the closest relatives of B. coli, as well as reference sequences of vestibuliferids. The SSrDNA tree showed the same phylogenetic diversification of B. coli at genus level as the tree constructed based on the ITS region. Based on the polymorphism of SSrDNA sequences, the type species of the genus, namely B. entozoon, appeared to be phylogenetically distinct from B. coli. Thus, we propose a new genus Neobalantidium for the homeothermic clade. Moreover, several isolates from both captive and wild primates (excluding great apes) clustered with B. sulcata with high support, suggesting the existence of a new species within this genus. The cysts of Buxtonella and Neobalantidium are morphologically indistinguishable and the presence of Buxtonella-like ciliates in primates opens the question about possible occurrence of these pathogens in humans.

Department of Pathology and Parasitology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Czech Republic

Zobrazit více v PubMed

Nakauchi K (1999) The prevalence of Balantidium coli in fifty-six mammalian species. J Vet Med Sci 6: 63–65. PubMed

Schuster FL, Ramirez-Avila L (2008) Current world status of Balantidium coli . Clin Microbiol Rev 21: 626–638. PubMed PMC

Areán VM, Koppisch E (1956) Balantidiasis. A review and report of cases. Am J Pathol 22: 1089–1115. PubMed PMC

Esteban JG, Aguirre C, Angles R, Ash L R, Mas-Coma R (1998) Balantidiasis in Aymara children from the Northern Bolivian Altiplano. Am J Trop Med Hyg 59: 922–927. PubMed

Owen IL (2005) Parasitic zoonosis in Papua New Guinea. J Helmint 79: 1–14. PubMed

Levecke B, Dorny P, Geurden T, Vercammen F, Vercruysse J (2007) Gastrointestinal protozoa in non-human primates of four zoological gardens in Belgium. Vet Parasitol 148: 236–246. PubMed

Pomajbíková K, Petrželková KJ, Profousová I, Petrášová J, Modrý D (2010) Discrepancies in the occurrence of Balantidium coli between captive and African great apes. J Parasitol 96: 1139–1144. PubMed

Weyher AH, Ross C, Semple S (2006) Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. Int J Primatol 27: 1519–1533.

Anargyrou K, Petrikkos GL, Suller MTE, Skiada A, Siakantaris MP, et al. (2003) Pulmonary Balantidium coli infection in a leukemic patient. Am J Hematol 73: 180–183. PubMed

Ferry T, Bouhour D, De Monbrison F, Laurent F, Dumouchel-Champagne H, et al. (2004) Severe peritonitis due to Balantidium coli acquired in France. Eur J Clin Microbiol Infect Dis 23: 393–395. PubMed

Maino A, Garigali G, Grande R, Messa P, Fogazzo GB (2010) Urinary balantidiasis: diagnosis at a glance by urine examination. J Nephrol 23: 732–737. PubMed

Cermeño JR, Hernández de Cuesta I, Uzcátegui O, Páez J, Rivera M, et al. (2003) Balantidium coli in an HIV-infected patient with chronic diarrhoea. AIDS 17: 941–2. PubMed

Clyti E, Aznar C, Couppie P, El Guedi M, Carme B, et al. (1998) Un cas de co-infection par Balantidium coli et VIH en Guayane Française. Bull Soc Pathol Exot 91: 309–311. PubMed

Hegner R (1934) Specificity in the genus Balantidium based on size and shape of body and macronucleus, with descriptions of six new species. Am J Epidemiol 19: 38–67.

Zaman V (1978) Balantidium coli, In: J.PKreier, editors. In: Parasitic Protozoa, vol. 2. New York: Academic Press. pp. 633–653.

Malmstein PH (1857) Infusorien als Intestinal-Thiere beim Menschen. Virchows Archiv für pathologische Anatomie und Physiologie und für klinische Medizin 12: 302–309.

Stein F (1863) Ueber Paramecium (?) coli Malmsten. Amtl Berl Dtsch Chem Ges 37: 165.

Claparède E, Lachmann J (1858) Balantidium entozoon. In: Études sur les infusoires et les Rhizopodes, Genève: Kossman. pp. 247.

Lynn D (2008) The ciliated protozoa. Characterization, classification and guide to the literature, 3rd ed. New York: Pergamon Press. 606 pp.

Quadri SS, Navarathnam S (1966) On a new species of Balantidium from an Indian monkey Macaca radiata . Riv Parassitol 27: 89–96. PubMed

Ponce-Gordo F, Jimenez_Ruiz E, Martínez-Díaz RA (2008) Tentative identification of the species of Balantidium from ostriches (Struthio camelus) as Balantidium coli-like by analysis of polymorphic DNA. Vet Parasitol 157: 41–49. PubMed

Cameron SL, Wright AG, O'Donoghue PJ (2003) An expanded phylogeny of the Entodiniomorphida (Ciliophora: Litostomatea). Acta Protozool 42: 1–6.

Strüder-Kypke MC, Kornilova OA, Lynn DH (2007) Phylogeny of trichostome ciliates (Ciliophora, Litostomatea) endosymbiotic in the Yakut horse (Equus caballus). Eur J Protistol 43: 319–328. PubMed

Vďačný P, Bourland WA, Orsi W, Epstein SS, Foissner W (2011) Phylogeny and classification of the Litostomatea (Protista, Ciliophora), with emphasis on free-living taxa and the 18S-rRNA gene. Mol Phylogenet Evol 59: 510–522. PubMed

Cameron SL (2002) Taxonomy and phylogeny of endosymbiotic ciliates (Ciliophora∶Litostomatea) associated with Australian herbivorous marsupials. Int J Parasitol 33: 347–355. PubMed

Nilles-Bije ML, Rivera WL (2010) Ultrastructural and molecular characterization of Balantidium coli isolated in the Philippines. Parasitol Res 106: 387–394. PubMed

Grim JN, Buonanno F (2009) A re-desription of the ciliate genus and type species, Balantidium entozoon . Eur J Protistol 45: 147–182. PubMed

Ponce-Gordo F, Fronseca-Salamanca F, Martínez-Díaz RA (2011) Genetic heterogeinity in internal transcribed spacer genes of Balantidium coli (Litostomatea, Ciliophora). Protist 162: 774–94. PubMed

Levecke B (2010) The occurrence of gastrointestinal parasites in captive non-human primates. In: The importance of gastrointestinal protozoa in captive non-human primates [dissertation]. Ghent University. pp. 72–93.

Lassmann T, Sonnhammer EL (2005) Kalign-an accurate and fast multiple sequence alignment algorithm. BMC bioinformatics 6: 298. PubMed PMC

Lassmann T, Sonnhammer EL (2006) Kalign, Kalignvu and Mumsa: web servers for multiple sequence alignment. Nucl Acids Res 34 Web Server issue: 596–9. PubMed PMC

Hall TA (1999) BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95–98.

Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307–21. PubMed

Lartillot N, Lepage T, Blanquart S (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25: 2286–2288. PubMed

Shimodaira H (2004) Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. Ann Stat 32: 2616–2641.

Stamatakis A (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690. PubMed

Shimodaira H, Hasegawa M (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17: 1246–1247. PubMed

Skotarczak B (1999) Cytochemical identification of mucocysts in Balantidium coli trophozoites. Folia Biol (Krakow) 47: 61–65. PubMed

Jameson AP (1926) A ciliate, Buxtonella sulcata n. g., n. sp., from the caecum of cattle. Parasitology 18: 182–186.

Lynn DH, Small EB (2000) Ciliophora, Litostomatea. In: Lee JJ, Leedale GF, Bradbury P, editors. An illustrated guide to the protozoa, second edition, vol I. Lawrence, USA: Allen Press Inc. 493–5 p.

Garcia LS (2008) Balantidium coli; In: Khan NA, editor. Emerging protozoan pathogens. New York: Taylor & Francis. 353–366 p.

Kennedy CC, Stewart TRC (1957) Balantidial dysentery: A human case in Northern Ireland. Trans R Soc Trop Med Hyg 51: 549–558. PubMed

Solaymani-Mohammadi S, Rezaian M, Anwar MA (2005) Human balantidiasis in Iran: an unresolved enigma? Trends Parasitol 21: 160–161. PubMed

Bakuza JS, Nkwengulila G (2009) Variation over time in parasite prevalence among free-rangin chimpanzees at Gombe National Park, Tanzania. Int J Primatol 30: 43–53.

Strüder-Kypke MC, Wright AD, Foissner W, Chatzinotas A, Lynn DH (2006) Molecular phylogeny of litostome ciliates (Cilophora, Litostomatea) with emphasis on free-living haptorian genera. Protist 157: 261–278. PubMed

Li M, Wang J, Zhang J, Gu Z, Ling F, et al. (2008) First report of two Balantidium species from the Chinese giant salamander, Andrias davidianus: Balantidium sinensis Nie 1935 and Balantidium andianusis n. sp. Parasitol Res 102: 605–611. PubMed

Fox MT, Jacobs DE (1986) Patterns of infection with Buxtonella sulcata in British cattle. Res Vet Sci 41: 90–92. PubMed

Lilly AA, Mehlman PT, Doran D (2002) Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park, Central African Republic. Int J Primatol 23: 555–573.

McGrew WC, Tutin CEG, Collins DA, File SK (1989) Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal). Am J Primatol 17: 147–155. PubMed

Vallo P, Petrželková KJ, Profousová I, Petrášová J, Pomajbíková K, et al. (2012) Molecular diversity of entodiniomorphid ciliate Troglodytella abrassarti and evaluation of its coevolution with chimpanzees. Am J Phys Anthropol 148 4: 525–33. PubMed

Wright AG (1999) Analysis of intraspecific sequence variation among eight isolate of the rumen symbiont, Isotricha protostoma (Ciliophora), from two continents. J Eukaryot Microbiol 46: 445–446. PubMed

Modrý D, Petrželková KJ, Pomajbíková K, Tokiwa T, Křížek J, et al. (2009) The occurrence and ape-to-ape transmission of the entodiniomorphid ciliates Troglodytella abrassarti in captive gorillas. J Eukaryot Microbiol 56: 83–87. PubMed

Williams AG, Coleman GS (1992) The rumen protozoa. New York: Springer Verlag. 441 p.

Bernhard D, Schlegel M (1998) Evolution of histone H4 and H3 genes in different ciliate lineages. J Mol Evol 46: 344–354. PubMed

Zhang Q, Simpson A, Song W (2012) Insigts into the phylogeny of systematically controversial haptorian ciliates (Ciliophora, Litostomatea) based on multigene analyses. Proc R Soc 279: 2625–2635. PubMed PMC

Tourancheau AB, Villalobo E, Tsao N, Torre A, Pearlman RE (1998) Protein coding gene trees in ciliates: comparison with rRNA-based phylogenies. Mol Phyl Evol 10: 299–309. PubMed

Israel R, Kosakovsky Pond SL, Muse SV, Katz LA (2002) Evolution of duplicated alpha-tubulin genes in ciliates. Evol 56: 1110–1122. PubMed

Association of human disturbance and gastrointestinal parasite infection of yellow baboons in western Tanzania

Parasitic Intestinal Protists of Zoonotic Relevance Detected in Pigs by Metabarcoding and Real-Time PCR

Are molecular tools clarifying or confusing our understanding of the public health threat from zoonotic enteric protozoa in wildlife?

Preliminary insights into the impact of dietary starch on the ciliate, Neobalantidium coli, in captive chimpanzees

Zobrazit více v PubMed

GENBANK
JQ073304, JQ073305, JQ073306, JQ073307, JQ073308, JQ073309, JQ073310, JQ073311, JQ073312, JQ073313, JQ073314, JQ073315, JQ073316, JQ073317, JQ073318, JQ073319, JQ073320, JQ073321, JQ073322, JQ073323, JQ073324, JQ073325, JQ073326, JQ073327, JQ073328, JQ073329, JQ073330, JQ073331, JQ073332, JQ073333, JQ073334, JQ073335, JQ073336, JQ073337, JQ073338, JQ073339, JQ073340, JQ073341, JQ073342, JQ073343, JQ073344, JQ073345, JQ073346, JQ073347, JQ073348, JQ073349, JQ073350, JQ073351, JQ073352, JQ073353, JQ073354, JQ073355, JQ073356, JQ073357, JQ073358, JQ073359, JQ073360, JQ073361, JQ073362, JQ073363, JQ073364, JQ073365, JQ073366, JQ073367, JQ073368, JQ073369, JQ073370, JQ073371, JQ073372, JQ073373, JQ073374, JQ073375, JQ073376, JQ073377, JQ073378, JQ073379, JQ073380, JQ073381, JQ073382, JQ073383, JQ073384, JQ073385, JQ073386, JQ073387, JQ408692, JQ408693, JQ408694