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Genetic diversity of cervid Trypanosoma theileri in Honshu sika deer (Cervus nippon) in Japan

Published online by Cambridge University Press:  27 July 2021

Imron Rosyadi
Affiliation:
Laboratory of Parasitology, Joint Graduate School of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
Aogu Setsuda
Affiliation:
Department of Pathological and Preventive Veterinary Science, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
Mafie Eliakunda
Affiliation:
Department of Pathological and Preventive Veterinary Science, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
Ai Takano
Affiliation:
Department of Pathological and Preventive Veterinary Science, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan Division of Pathogenic Microorganisms, Research Center for Thermotolerant Microbial Resources, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
Ken Maeda
Affiliation:
Department of Pathological and Preventive Veterinary Science, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan Division of Pathogenic Microorganisms, Research Center for Thermotolerant Microbial Resources, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
Atsuko Saito-Ito
Affiliation:
Section of Microbiology, School of Pharmacy, Hyogo University of Health Sciences, 1-3-6 Minatojima, Chuo-ku, Kobe, Hyogo650-8530, Japan
Kazuo Suzuki
Affiliation:
Hikiiwa Park Center, 1629 Inari-cho, Tanabe, Wakayama646-0051, Japan
Hiroshi Sato*
Affiliation:
Laboratory of Parasitology, Joint Graduate School of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan Department of Pathological and Preventive Veterinary Science, United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan Division of Pathogenic Microorganisms, Research Center for Thermotolerant Microbial Resources, Yamaguchi University, 1677-1 Yoshida, Yamaguchi753-8515, Japan
*
Author for correspondence: Hiroshi Sato, E-mail: sato7dp4@yamaguchi-u.ac.jp

Abstract

The taxonomy of ruminant Trypanosoma theileri and its relatives (Kinetoplastida: Trypanosomatidae) is controversial, with recent phylogenetic studies segregating T. theileri in cattle and other ruminants worldwide into two major genetic lineages (the TthI and TthII clades) based on genetic markers. In the present study, T. theileri-like trypanosomes isolated from Honshu sika deer (Cervus nippon) in the western Japan (YMG isolate) were genetically characterized using a number of genetic markers. Sika deer trypanosomes of the YMG isolate were genetically different from the Trypanosoma sp. TSD1 isolate previously recorded from Hokkaido sika deer in northern Japan, with the former trypanosome isolate being genetically closer to European cervid trypanosomes and the bovine T. theileri TthII lineage. In contrast, the latter isolate exhibited greater relatedness to North American cervid trypanosomes and the bovine T. theileri TthI lineage, although a clear genetic distinction between these was apparent. Furthermore, trypanosomes in Honshu sika deer from the central part of Japan harboured additional genetic diversity and were closer to either TSD1 or YMG isolates, while distinct from known T. theileri-related genotypes. Importantly, cervids and wild ruminants worldwide might harbour divergent descendants of a T. theileri ancestor, which exhibit rigid host specificity to either bovines or cervid species.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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Footnotes

*

These two authors contributed equally to this work.

References

Anisimova, M and Gascuel, O (2006) Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539552.CrossRefGoogle ScholarPubMed
Auty, H, Anderson, NE, Picozzi, K, Lembo, T, Mubanga, J, Hoare, R, Fyumagwa, RD, Mable, B, Hamill, L, Cleaveland, S and Welburn, SC (2012) Trypanosome diversity in wildlife species from the Serengeti and Luangwa Valley ecosystems. PLoS Neglected Tropical Diseases 6, e1828.CrossRefGoogle ScholarPubMed
Böse, R, Friedhoff, KT and Olbrich, S (1987 a) Transmission of Megatrypanum trypanosomes to Cervus dama by Tabanidae. Journal of Protozoology 34, 110113.CrossRefGoogle ScholarPubMed
Böse, R, Friedhoff, KT, Olbrich, S, Büscher, G and Domeyer, I (1987 b) Transmission of Trypanosoma theileri to cattle by Tabanidae. Parasitology Research 73, 421424.CrossRefGoogle ScholarPubMed
Böse, R, Petersen, K, Pospichal, H, Buchanan, N and Tait, A (1993) Characterization of Megatrypanum trypanosomes from European Cervidae. Parasitology 107, 5561.CrossRefGoogle ScholarPubMed
Cortez, AP, Rodrigues, AC, Garcia, HA, Neves, L, Batista, JS, Bengaly, Z, Paiva, F and Teixeira, MMG (2009) Cathepsin L-like genes of Trypanosoma vivax from Africa and South America – characterization, relationships and diagnostic implications. Molecular and Cellular Probes 23, 4451.CrossRefGoogle ScholarPubMed
D'Alessandro, PA and Behr, MA (1991) Trypanosoma lewisi and its relatives. In Kreier, JP and Baker, JR (eds), Parasitic Protozoa 2nd Edn. vol 1. San Diego, CA, USA: Academic Press, pp. 225263.Google Scholar
Dereeper, A, Guignon, V, Blanc, G, Audic, S, Buffet, S, Chevenet, F, Dufayard, JF, Guindon, S, Lefort, V, Lescot, M, Claverie, J-M and Gascuel, O (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, 465469.CrossRefGoogle ScholarPubMed
Dirie, MF, Bornstein, S, Wallbanks, KR, Molyneux, DH and Steen, M (1990) Comparative studies on Megatrypanum trypanosomes from cervids. Tropical Medicine and Parasitology 41, 198202.Google ScholarPubMed
Ellis, J, Barratt, J, Kaufer, A, Pearn, L, Armstrong, B, Johnson, M, Park, Y, Downey, L, Cao, M, Neill, L, Lee, R, Ellis, B, Tyler, K, Lun, Z-R and Stark, D (2021) A new subspecies of Trypanosoma cyclops found in the Australian terrestrial leech Chtonobdella bilineata. Parasitology 148, 11251136.CrossRefGoogle ScholarPubMed
Fisher, AC, Schuster, G, Cobb, WJ, James, AM, Cooper, SM, Peréz de León, AA and Holman, PJ (2013) Molecular characterization of Trypanosoma (Megatrypanum) spp. infecting cattle (Bos taurus), white-tailed deer (Odocoileus virginianus), and elk (Cervus elaphus canadensis) in the United States. Veterinary Parasitology 197, 2942.CrossRefGoogle Scholar
Garcia, HA, Kamyingkird, K, Rodrigues, AC, Jittapalapong, S, Teixeira, MMG and Desquesnes, M (2011 a) High genetic diversity in field isolates of Trypanosoma theileri assessed by analysis of cathepsin L-like sequences disclosed multiple and new genotypes infecting cattle in Thailand. Veterinary Parasitology 180, 363367.CrossRefGoogle ScholarPubMed
Garcia, HA, Rodrigues, AC, Martinkovic, F, Minervino, AHH, Campaner, M, Nunes, VLB, Paiva, F, Hamilton, PB and Teixeira, MMG (2011 b) Multilocus phylogeographical analysis of Trypanosoma (Megatrypanum) genotypes from sympatric cattle and water buffalo populations supports evolutionary host constraint and close phylogenetic relationships with genotypes found in other ruminants. International Journal for Parasitology 41, 13851396.CrossRefGoogle ScholarPubMed
Garcia, HA, Blanco, PA, Rodrigues, AC, Rodrigues, CMF, Carmen, SA, Takata, CSA, Campaner, M, Camargo, EP and Teixeira, MMG (2020) Pan-American Trypanosoma (Megatrypanum) trinaperronei n. sp. in the white tailed deer Odocoileus virginianus Zimmermann and its deer ked Lipoptena mazamae Rondani, 1878: morphological, developmental and phylogeographical characterization. Parasites & Vectors 13, 308.CrossRefGoogle Scholar
Gibson, W, Pilkington, JG and Pemberton, JM (2010) Trypanosoma melophagium from the sheep ked Melophagus ovinus on the island of St Kilda. Parasitology 137, 17991804.CrossRefGoogle ScholarPubMed
Guindon, S and Gascuel, O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.CrossRefGoogle ScholarPubMed
Hamilton, PB, Stevens, JR, Gaunt, MW, Gidley, J and Gibson, WC (2004) Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. International Journal for Parasitology 34, 13931404.CrossRefGoogle ScholarPubMed
Hamilton, PB, Stevens, JR, Gidley, J, Holz, P and Gibson, WC (2005) A new lineage of trypanosomes from Australian vertebrates and terrestrial bloodsucking leeches (Haemadipsidae). International Journal for Parasitology 35, 431443.CrossRefGoogle Scholar
Hamilton, PB, Stevens, JR and Gibson, WC (2007) Patterns of co-evolution between trypanosomes and their hosts deduced from ribosomal RNA and protein-coding gene phylogenies. Molecular Phylogenetics and Evolution 44, 1525.CrossRefGoogle ScholarPubMed
Hamilton, PB, Adams, ER, Njiolou, F, Gibson, WC, Cuny, G and Herder, S (2009) Phylogenetic analysis reveals the presence of the Trypanosoma cruzi clade in African terrestrial mammals. Infection, Genetics and Evolution 9, 8186.CrossRefGoogle ScholarPubMed
Hatama, S, Shibahara, T, Muzuki, M, Kadota, K, Uchida, I and Kanno, T (2007) Isolation of a Megatrypanum trypanosome from sika deer (Cervus nippon yesoensis) in Japan. Veterinary Parasitology 149, 5664.CrossRefGoogle ScholarPubMed
Hoare, CA (1972) The Trypanosomes of Mammals: A Zoological Monograph. Oxford, UK: Blackwell Scientific Publications.Google Scholar
Kingston, N and Morton, JK (1975) Trypanosoma cervi sp. n. from elk (Cervus canadensis) in Wyoming. Journal of Parasitology 61, 1723.CrossRefGoogle Scholar
Kingston, N, Franzmann, A and Maki, L (1985) Redescription of Trypanosoma cervi (Protozoa) in moose, Alces alces, from Alaska and Wyoming. Proceedings of the Helminthological Society of Washington 52, 5459.Google Scholar
Kingston, N, Thomas, G, McHolland, L, Williams, ES, Trueblood, MS and Maki, L (1986) Experimental transmission of Trypanosoma theileri to bison. Proceedings of the Helminthological Society of Washington 53, 198203.Google Scholar
Kingston, N, Bobek, B and Perzanowski, K (1992) Description of Trypanosoma (Megatrypanum) stefanskii sp. n. from roe deer (Capreolus capreolus) in Poland. Journal of the Helminthological Society of Washington 59, 8995.Google Scholar
Martinković, F, Matanović, K, Rodrigues, AC, Garcia, HA and Teixeira, MMG (2012) Trypanosoma (Megatrypanum) melophagium in the sheep ked Melophagus ovinus from organic farms in Croatia: phylogenetic inferences support restriction to sheep and sheep keds and close relationship with trypanosomes from other ruminant species. Journal of Eukaryotic Microbiology 59, 134144.CrossRefGoogle ScholarPubMed
Nagata, J, Masuda, R, Tamate, HB, Hamasaki, S, Ochiai, K, Asada, M, Tatsuzawa, S, Suda, K, Tado, H and Yoshida, MC (1999) Two genetically distinct lineages of the sika deer, Cervus nippon, in Japanese Islands: comparison of mitochondrial D-loop region sequences. Molecular Phylogenetics and Evolution 13, 511519.CrossRefGoogle ScholarPubMed
Ohdachi, SD, Ishibashi, Y, Iwasa, MA and Saitoh, T (2010) The Wild Mammals of Japan. Kyoto, Japan: Shoukadoh Book Sellers.Google Scholar
Pacheco, TDA, Marcili, A, da Costa, AP, Witter, R, Melo, ALT, Boas, RV, Chitarra, CS, Dutra, V, Nakazato, L and Pacheco, RC (2018) Genetic diversity and molecular survey of Trypanosoma (Megatrypanum) theileri in cattle in Brazil's western Amazon region. Revista Brasileira de Parasitologia Veterinária 27, 579583.CrossRefGoogle ScholarPubMed
Rodrigues, AC, Campaner, M, Takata, CS, Dell'Porto, A, Milder, RV, Takeda, GF and Teixeira, MMG (2003). Brazilian isolates of Trypanosoma (Megatrypanum) theileri: diagnosis and differentiation of isolates from cattle and water buffalo based on biological characteristics and randomly amplified DNA sequences. Veterinary Parasitology 116, 185207.CrossRefGoogle ScholarPubMed
Rodrigues, AC, Paiva, F, Campaner, M, Stevens, JR, Noyes, HA and Teixeira, MMG (2006) Phylogeny of Trypanosoma (Megatrypanum) theileri and related trypanosomes reveals lineages of isolates associated with artiodactyl hosts diverging on SSU and ITS ribosomal sequences. Parasitology 132, 215224.CrossRefGoogle ScholarPubMed
Rodrigues, AC, Garcia, HA, Batista, JS, Minervino, AHH, Góes-Cavalcante, GG, Silva, FMD, Ferreira, RC, Campaner, M, Paiva, F and Teixeira, MMG (2010 a) Characterization of spliced leader genes of Trypanosoma (Megatrypanum) theileri: phylogeographical analysis of Brazilian isolates from cattle supports spatial clustering of genotypes and parity with ribosomal markers. Parasitology 137, 111122.CrossRefGoogle ScholarPubMed
Rodrigues, AC, Garcia, HA, Ortiz, PA, Cortez, AP, Martinkovic, F, Paiva, F, Batista, JS, Minervino, AH, Campaner, M, Pral, EM, Alfieri, SC and Teixeira, MMG (2010 b) Cysteine proteases of Trypanosoma (Megatrypanum) theileri: cathepsin L-like gene sequences as targets for phylogenetic analysis, genotyping diagnosis. Parasitology International 59, 318325.CrossRefGoogle ScholarPubMed
Sato, H, Ishita, K, Matsuo, K, Inaba, T, Kamiya, H and Ito, M (2003) Persistent infection of Mongolian jirds with a non-pathogenic trypanosome, Trypanosoma (Herpetosoma) grosi. Parasitology 127, 357363.CrossRefGoogle ScholarPubMed
Sato, H, Osanai, A, Kamiya, H, Obara, Y, Jiang, W, Zhen, W, Chai, J, Une, Y and Ito, M (2005) Characterization of SSU and LSU rRNA genes of three Trypanosoma (Herpetosoma) grosi isolates maintained in Mongolian jirds. Parasitology 130, 157167.CrossRefGoogle ScholarPubMed
Sato, H, Leo, N, Katakai, Y, Takano, J, Akari, H, Nakamura, S and Une, Y (2008) Prevalence and molecular phylogenetic characterization of Trypanosoma (Megatrypanum) minasense in the peripheral blood of small Neotropical primates after a quarantine period. Journal of Parasitology 94, 11281138.CrossRefGoogle ScholarPubMed
Schlafer, DH (1979) Trypanosoma theileri: a literature review and report of incidence in New York cattle. Cornell Veterinarian 69, 411425.Google ScholarPubMed
Stevens, J, Teixeira, MMG, Bingle, LEH and Gibson, WC (1999) The taxonomic position and evolutionary relationships of Trypanosoma rangeli. International Journal for Parasitology 29, 749757.CrossRefGoogle ScholarPubMed
Tamate, HB, Tatsuzawa, S, Suda, K, Izawa, M, Doi, T, Sunagawa, K, Miyahira, F and Tado, H (1998) Mitochondrial DNA variations in local populations of the Japanese sika deer, Cervus nippon. Journal of Mammalogy 79, 13961403.CrossRefGoogle Scholar
Teacher, AGF and Griffiths, DJ (2011) HapStar: automated haplotype network layout and visualization. Molecular Ecology Resources 11, 151153.CrossRefGoogle ScholarPubMed
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.CrossRefGoogle ScholarPubMed
Thompson, CK, Godfrey, SS and Thompson, RCA (2014) Trypanosomes of Australian mammals: a review. International Journal for Parasitology: Parasites and Wildlife 3, 5766.Google ScholarPubMed
Touré, S (1968) Description complémentaire de Trypanosoma theileri Laveran, 1902. Mention particulière des formes observées en Casamance (Sénégal). Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux 21, 365373.Google Scholar
Votýpka, J, d'Avila-Levy, CM, Grellier, P, Maslov, DA, Lukeš, J and Yurchenko, V (2015) New approaches to systematics of Trypanosomatidae: criteria for taxonomic (re)description. Trends in Parasitology 31, 460469.CrossRefGoogle ScholarPubMed
Weerasooriya, G, Sivakumar, T, Lan, DTB, Long, PT, Takemae, H, Igarashi, I, Inoue, N and Yokoyama, N (2016) Epidemiology of bovine hemoprotozoa parasites in cattle and water buffalo in Vietnam. Journal of Veterinary Medical Science 78, 13611367.CrossRefGoogle ScholarPubMed
Wita, I and Kingston, N (1999) Trypanosoma cervi in red deer, Cervus elaphus, in Poland. Acta Parasitologica 44, 9398.Google Scholar
Ybañez, AP, Sivakumar, T, Ybañez, RH, Vincoy, MR, Tingson, JA, Perez, ZO, Gabotero, SR, Buchorno, LP, Inoue, N, Matsumoto, K, Inokuma, H and Yokoyama, N (2013) Molecular survey of bovine vector-borne pathogens in Cebu, Philippines. Veterinary Parasitology 196, 1320.CrossRefGoogle ScholarPubMed
Yokoyama, N, Sivakumar, T, Fukushi, S, Tattiyapong, M, Tuvshintulga, B, Kothalawala, H, Silva, SS, Igarashi, I and Inoue, N (2015) Genetic diversity in Trypanosoma theileri from Sri Lankan cattle and water buffaloes. Veterinary Parasitology 207, 335341.CrossRefGoogle ScholarPubMed
Zuker, M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31, 34063415.CrossRefGoogle ScholarPubMed
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