De Novo Transcriptome Analysis of Oncomelania hupensis after Molluscicide Treatment by Next-Generation Sequencing: Implications for Biology and Future Snail Interventions

Abstract

The freshwater snail Oncomelania hupensis is the only intermediate host of Schistosoma japonicum, which causes schistosomiasis. This disease is endemic in the Far East, especially in mainland China. Because niclosamide is the only molluscicide recommended by the World Health Organization, 50% wettable powder of niclosamide ethanolamine salt (WPN), the only chemical molluscicide available in China, has been widely used as the main snail control method for over two decades. Recently, a novel molluscicide derived from niclosamide, the salt of quinoid-2',5-dichloro-4'-nitro-salicylanilide (Liu Dai Shui Yang An, LDS), has been developed and proven to have the same molluscicidal effect as WPN, with lower cost and significantly lower toxicity to fish than WPN. The mechanism by which these molluscicides cause snail death is not known. Here, we report the next-generation transcriptome sequencing of O. hupensis; 145,008,667 clean reads were generated and assembled into 254,286 unigenes. Using GO and KEGG databases, 14,860 unigenes were assigned GO annotations and 4,686 unigenes were mapped to 250 KEGG pathways. Many sequences involved in key processes associated with biological regulation and innate immunity have been identified. After the snails were exposed to LDS and WPN, 254 unigenes showed significant differential expression. These genes were shown to be involved in cell structure defects and the inhibition of neurohumoral transmission and energy metabolism, which may cause snail death. Gene expression patterns differed after exposure to LDS and WPN, and these differences must be elucidated by the identification and annotation of these unknown unigenes. We believe that this first large-scale transcriptome dataset for O. hupensis will provide an opportunity for the in-depth analysis of this biomedically important freshwater snail at the molecular level and accelerate studies of the O. hupensis genome. The data elucidating the molluscicidal mechanism will be of great benefit in future snail control efforts.

Altered Gene Expression in the Schistosome-Transmitting Snail Biomphalaria glabrata following Exposure to Niclosamide, the Active Ingredient in the Widely Used Molluscicide Bayluscide

“…Based on Illumina RNA-seq analysis, Zhao et al (2015) described the responses of the amphibious snail, Oncomelania hupensis , after challenge with two different niclosamide-based molluscicides. They showed that two CYP genes and one GST gene were upregulated following molluscicide exposure [ 51 ]. This observation coupled with our results suggests that both enzyme families are a common component of the snail transcriptomic response to molluscicides.…”

Transcriptional responses ofBiomphalaria pfeifferiandSchistosoma mansonifollowing exposure to niclosamide, with evidence for a synergistic effect on snails following exposure to both stressors

“…Zhao et al [15] undertook an Illumina-based study of the molluscicide-induced transcriptome of Oncomelania hupensis, the pomatiopsid snail host of S. japonicum. The response of B. pfeifferi to simultaneous exposure to schistosome infection and niclosamide exposure is the first glimpse we have for how snails respond transcriptionally to simultaneous exposure to these two relevant stressors.…”

“…CYPs are also up-regulated in B. pfeifferi in response to niclosamide exposure, including two in common with B. glabrata ( Table 1) Glutathione-S-transferase 7-like (GST) was up-regulated 5-fold following niclosamide exposure in B. glabrata [16]. In addition to CYPs, GST has also been shown to be upregulated following niclosamide-based molluscicide exposure in Oncomelania hupensis [15].…”

Temporal transcriptome change of Oncomelania hupensis revealed by Schistosoma japonicum invasion

“…By contrast, only a few study focused on the transcriptomic studies in the snail O. hupensis, for instance, Zhao et al have characterized the transcriptome profiling of O. hupensis from the two distinct habitats and identified thousands of genes that show either increased or decreased expression [15]. A RNA-Seq experiment revealed that gene expression of O. hupensis showed significantly effects exposed to two kinds of molluscicides [14]. Together these data demonstrate the highly dynamic nature of transcriptomic profile in response to environment, infection and molluscicide.…”

“…For O. hupensis, transcriptomic studies by RNA-seq have been performed after molluscicide treatment. Many genes involved in key processes associated with biological regulation and innate immunity have been identified, which would benefit for elucidating the molluscicidal mechanism [14]. Another study by comparing the differences in gene expression between the hilly and marshland snails revealed that there is a potential relationship between expression profiling and ecological adaptation of the snail that may have implications for schistosomiasis control in future [15].…”