Pathologic, transcriptomic and microbiomic insight into the pathogenesis of intestinal parasitic tapeworm in cultured Chinese soft-shelled turtle (Pelodiscus sinensis)

Abstract

Tapeworms are infamous and highly successful invasive parasites in aquatic animals, especially in fish. However, tapeworm-caused diseases in soft-shelled turtles are rarely discovered. In this study, a case of cultured Chinese soft-shelled turtle (Pelodiscus sinensis) infected with tapeworm in Changde city of China was reported, and the taxonomic identification of the tapeworm and the effects of tapeworm on the Chinese soft-shelled turtle were revealed. The 28S rRNA sequences of the tapeworm from P. sinensis had the highest similarity (99.82%) with Testudotaenia testudo of Proteocephalidea (Eucestoda), suggesting they are identical species. Infected turtles showed typical clinical symptoms of cestodiasis, which included nutrition loss, and histopathological lesions in the liver and intestine. The serum of infected turtles had significantly lower (P < 0.05) concentrations of glucose, creatinine, total protein, and low-density lipoprotein, and significantly higher (P < 0.05) alanine transaminase (ALT), aspartate transaminase (AST), alkaline phosphatase (ALP), superoxide dismutase (SOD) activities. Trancriptional analyses showed that 158 differentially expressed genes (DEGs) were found in liver of infected turtles compared with uninfected groups. These DEGs mainly involved in metabolism, including “Arachidonic acid metabolism”, “Linoleic acid metabolism”, “Metabolism of xenobiotics by cytochrome P450”, “alpha-Linolenic acid metabolism”, “Ether lipid metabolism”, “Retinol metabolism” and “Glycerophospholipid metabolism”, which suggested that the tapeworm infection seriously affected the nutrient metabolism of P. sinensis. Besides, 12 immune-related DEGs were discovered and 7 of them were down-regulated, which inferred that tapeworm may regulate immune responses of host. Gut microflora analysis showed that there were no significant differences in richness and diversity between the infected and uninfected groups. Nevertheless, some opportunistic pathogens such as Citrobacter, Edwardsiella, and Lawsonia were significant higher (P < 0.05) in infected turtles, and the intestinal microflora in infected turtles were associated with “Bacterial invasion of epithelial cells” based on functional prediction. Overall, our results suggested that the tapeworm infection caused mechanical damage in the intestine, metabolism disorder in liver, and increased abundance of pathogenic bacteria in gut microflora. Our results provided a first insight into the pathogenesis of tapeworm infection in the Chinese soft-shelled turtle.