First report of Schistosoma sinensium infecting Tupaia belangeri and Tricula sp. LF

Abstract

Schistosoma sinensium belongs to the Asian Schistosoma and is transmitted by freshwater snails of the genus Tricula. Rodents are known definitive hosts of S. sinensium. In 2016, suspected schistosome eggs were found in the feces of the northern tree shrew (Tupaia belangeri) in a field in Lufeng County (latitude, 25°04'50″ N; longitude, 102°19'30″ E; altitude 1820 m), Yunnan Province, China. Morphological analysis suggested that the schistosome was S. sinensium. 18S, 12S and CO1 genes sequencing and phylogenetic analysis showed that this species had the highest similarity to and occupied the same evolutionary branch as S. sinensium from Mianzhu, Sichuan, China. Meanwhile, based on 16S and 28S rDNA sequencing and morphological identification, the snail intermediate host was identified as a species of Tricula, and was found in irrigation channels. Phylogeny indicated that Tricula sp. LF was a sister taxon to T. bambooensis, T. ludongbini. The S. sinensium was able to experimentally infect the captive-bred Tupaia belangeri, and Schistosoma eggs were recovered from all Tupaia belangeri exposed. In this study, we report the infection of Tupaia belangeri and Tricula sp. LF with S. sinensium in Lufeng, Yunnan, southwest China. These findings may improve our understanding of the host range, evolution, distribution, and phylogenetic position of S. sinensium.

Keywords: Schistosoma sinensium; Tricula sp. LF; Tupaia belangeri.

Fig. 1

Morphology of S. sinensium at different life cycle stages. Miracidia and cercariae were stained with iodine. A. Egg. B. Miracidium. C. Cercaria. D. Male and female adult worms.

Fig. 2

Enlarged worm picture. A. Male, showing oral sucker (os), ventral sucker (vs), constriction (pac), testes (te), gut caeca (int) and gynecophoral canal (gyn). B. Female, showing oral sucker (os), ventral sucker (vs), utero (ut), ovary(ov), vitellarium (vg) and gut caeca (int).

Fig. 3

Molecular phylogenetic analyses of the present Schistosoma sinensium (♦) by the maximum likelihood method (ML) and maximum parsimony method (MP). Phylogenetic tree depicting relationships among Schistosoma species inferred from: A. 18S nucleotide data analyses using ML (Ai) and MP (Aii). [Schistosoma malayensis AY157227.1, Schistosoma mekongi AY157228.1, Schistosoma sinensium AY157225.1, Schistosoma indicum AY157231.1 and Schistosoma japonicum AY157226.1 were cited from Lockyer et al. (2003); Schistosoma incognitum JQ408706.1 was cited from Webster and Littlewood (2012); Schistosoma.spindale Z11979.1 was cited from Johnston et al. (1993)]. B. CO1 nucleotide data analyses using ML (Bi) and MP (Bii). [Schistosoma malayensis AY157198.1, Schistosoma mekongi AY157199.1, Schistosoma sinensium AY157197.1 and Schistosoma incognitum AY157201.1 were cited from Lockyer et al. (2003); Schistosoma indicum NC_047240.1 was cited from Jones et al. (2020); Schistosoma nasale KR607232.1 was cited from Devkota et al. (2015)]. C.12S nucleotide data analyses using ML (Ci) and MP (Cii). [Schistosoma mekongi AF217449.1 was cited from Le et al. (2000); Schistosoma sinensium AF465918.1 and Schistosoma ovuncatum AF465917.1 were cited from Attwood et al. (2002a); Schistosoma incognitum EF534279.1 was cited from Attwood et al. (2007); Schistosoma nasale KR607261.1 was cited from Devkota et al. (2015); Schistosoma mansoni MN593407.1 was cited from Catalano et al. (2020); Schistosoma indicum NC_047240.1 and Schistosoma spindale MN637820.1 were cited from Jones et al. (2020)]. Other sequences were from GenBank.

Fig. 4

Shell morphology of Tricula sp. LF. A. Shape. B–C. Scanning electron micrograph of the radula.

Fig. 5

Molecular phylogenetic analyses of the Tricula sp. LF (♦) by the maximum likelihood method (ML) and maximum parsimony method (MP). Phylogenetic tree depicting relationships among Tricula species inferred from: A. 28S nucleotide data analyses using ML (Ai) and MP (Aii). [Tricula ludongbini AY207037.1, Tricula bambooensis AY207036.1, Tricula xiaolongmenensis AY207040.1, Neotricula aperta AY207034.1 and Delavaya dianchiensis AY207038.1 were cited from Attwood et al. (2004); Gammatricula shini AB611797.1 was cited from Kameda and Kato (2011)]. Outgroup taxon Potamopyrgus antipodarum-JF960454.1. B. 16S nucleotide data analyses using ML (Bi) and MP (Bii). [Tricula ludongbini AY207031.1, Tricula bambooensis AY207030.1, Delavaya dianchiensis AY207033.1 and Tricula xiaolongmenensis AY207032.1 were cited from Attwood et al. (2004); Tricula hudiequanensis KC832712.1 and Jinghongia jinghongensis KC832728.1 were cited from Liu et al. (2014); Neotricula aperta EU306250.1 was cited from Attwood et al. (2008); Gammatricula shini AB611798.1 was cited from Kameda and Kato (2011)]. Outgroup taxon Potamopyrgus antipodarum-AY314009.1. Other sequences were from GenBank.