Abstract
Four adult female worms of Trichuris were isolated from an individual of the wild blue sheep (Pseudois nayaur) inhabiting the Helan Mountains, China, during an epidemiological survey of this wild ruminant. Although there were some differences among the worms in posterior end (rectum) morphology and egg shape, little information regarding species status could be inferred from their morphology. Phylogenetic trees were constructed based on sequences of the ITS1 segment of ribosomal RNA (rRNA), and the sequences of the four Trichuris specimens from wild blue sheep were divided into two distinct lineages (Clade A and Clade B). The two specimens in Clade A were named Genotype I, and had the closest relationship with Trichuris skrjabini; the two specimens in Clade B were named Genotype II and had the closest genetic relationship with a previously described Trichuris sp. In the two Trichuris genotypes identified in the present study, the 18S fragments (261 to 262 bp) of the newly obtained sequences were found to be highly conserved, with merely one insert mutation of a single nucleotide present. The genetic distance based on ITS1 between members of Clade A, composed of two T. skrjabini individuals and two Genotype I individuals, ranged from 0 to 0.0034. These distances are within the intraspecies variation of Trichuris (0–0.0272), suggesting that the Genotype I individuals infesting the wild blue sheep were T. skrjabini. In Clade B, the newly obtained sequences clustered with Trichuris sp. specimens isolated from ruminants (sheep and black goat) with strong support, and the genetic distance ranged from 0.0068 to 0.017, which is also within the intraspecies variation of Trichuris (0–0.0272). However, the genetic distances between the Clade A and Clade B were 0.0442 to 0.0578, which are higher than the intraspecies distances in Trichuris but lower than the interspecies distances (0.102–0.5078). These results implied that Clade A and Clade B most likely represent two subpopulations of T. skrjabini; however, the possibility that Clade A is T. skrjabini and Clade B is a Candidatus Trichuris could not be excluded.
Data availability
All data from this study are available.
References
Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75. https://doi.org/10.1038/32160
Callejón R, Nadler S, De Rojas M, Zurita A, Petrasova J, Cutillas C (2013) Molecular characterization and phylogeny of whipworm nematodes inferred from DNA sequences of cox1 mtDNA and 18S Rdna. Parasitol Res 112:3933–3949. https://doi.org/10.1007/s00436-013-3584-z
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Cutillas C, Callejon R, de Rojas M, Tewes B, Ubeda JM, Ariza C, Guevara DC (2009) Trichuris suis and Trichuris trichiura are different nematode species. Acta Trop 111:299–307. https://doi.org/10.1016/j.actatropica.2009.05.011
Cutillas C, de Rojas M, Zurita A, Oliveros R, Callejon R (2014) Trichuris colobae n. sp. (Nematoda: Trichuridae), a new species of Trichuris from Colobus guereza kikuyensis. Parasitol Res 113:2725–2732. https://doi.org/10.1007/s00436-014-3933-6
Cutillas C, Oliveros R, de Rojas M, Guevara DC (2002) Determination of Trichuris muris from murid hosts and T. arvicolae (Nematoda) from arvicolid rodents by amplification and sequentiation of the ITS1-5.8S-ITS2 segment of the ribosomal DNA. Parasitol Res 88:574–582. https://doi.org/10.1007/s00436-002-0596-5
Cutillas C, Oliveros R, de Rojas M, Guevara DC (2004) Determination of Trichuris skrjabini by sequencing of the ITS1-5.8S-ITS2 segment of the ribosomal DNA: comparative molecular study of different species of trichurids. J Parasitol 90:648–652. https://doi.org/10.1645/GE-3295RN
Gagarin VG (1974) On the technique of evaluation of anthelmintics effectiveness. Biull Vses Ordena Tr Krasnogo Znameni Inst Gelmintol 12:23–26
Ghai RR, Simons ND, Chaoman CA, Omeja PA, Davies TJ, Ting N, Goldberg TL (2014) Hidden population structure and cross-species transmission of whipworms (Trichuris sp.) in humans and non-human primates in Uganda. PLoS Negl Trop Dis 8(10):e3256. https://doi.org/10.1371/journal.pntd.0003256
Guardone L, Deplazes P, Macchioni F, Magi M, Mathis A (2013) Ribosomal and mitochondrial DNA analysis of Trichuridae nematodes of carnivores and small mammals. Vet Parasitol 197:364–369. https://doi.org/10.1016/j.vetpar.2013.06.022
Holterman M, van der Wuff A, van den Elsen S, van Megen H, Bongers T, Holovachow O, Bakker J, Helder J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown. Clades Mol Biol Evol 23:1792–1800. https://doi.org/10.1093/molbev/msl044
Knight RA (1984) Morphological differences in Trichuris ovis associated with different host species. J Parasitol 70:842–843
Polley L (2002) Parasitic diseases of wild mammals. Can Vet J 43:130
Robles Mdel R, Navone GT, Notarnicola J (2006) A new species of Trichuris (Nematoda: Trichuridae) from Phyllotini rodents in Argentina. J Parasitol 92:100–104. https://doi.org/10.1645/ge-ge-552r.1
Roepstorff A, Mejer H, Nejsum P, Thamsborg SM (2011) Helminth parasites in pigs: new challenges in pig production and current research highlights. Vet Parasitol 18:72–81. https://doi.org/10.1016/j.vetpar.2011.05.029
Subbotin SA, Vierstraete A, De Ley P, Rowe J, Waeyenberge L, Moens M, Vanfleteren JR (2001) Phylogenetic relationships within the cyst-forming nematodes (Nematoda, Heteroderidae) based on analysis of sequences from the ITS regions of ribosomal DNA. Mol Phylogenet Evol 21:1–16. https://doi.org/10.1006/mpev.2001.0998
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This study was supported by grants from the following: the National Natural Science Foundation of China (31870512) and Surveillance of Wildlife Diseases from the State Forestry Administration of China.
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LWT, ZSL, and ZJH conceived the project. MCZ and DDS designed the experiments. JFW, YL, YS, ZWP, and MCZ performed the experiments. DDS carried out the data analysis. MCZ and DDS wrote the manuscript.
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We declare that all the wild blue sheep in current work were culled from the population by local Helan Mountains’ government agents. There is no conflict of interest with species conservation guidelines. The collection of the worms from the wild sheep was approved by the local Helan government agents. All experimental designs and animal handling were approved by the Institutional Animal Care and Use Committee of Northeast Forestry University.
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Zhou, M., Shen, D., Wang, J. et al. First isolation of Trichuris from wild blue sheep (Pseudois nayaur) in the Helan Mountains, China. Parasitol Res 120, 2665–2670 (2021). https://doi.org/10.1007/s00436-021-07192-x
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DOI: https://doi.org/10.1007/s00436-021-07192-x