Gender-specific metabolic responses in gonad of mussel Perna viridis to triazophos

Highlights

• This work confirmed apparent gender-specific responses in P. viridis to triazophos.

• Triazophos caused disruption of energy metabolism and osmotic regulation in ovaries.

• In testises, triazophos only caused disturbance in energy metabolism.

• Potential gender-neutral & gender-specific biomarkers were selected for triazophos.

Abstract

Triazophos, as a lipophilic organophosphate pesticide, displays higher bioaccumulation in the gonads of shellfish. To study the reproductive toxicity of triazophos, we applied metabolomics to characterize the gender-specific metabolic responses in mussel Perna viridis exposed to triazophos. Metabolites were differently altered by triazophos in ovaries of mussel at different concentrations and time intervals, while basically similar metabolic response patterns were observed in male mussels at the two tested concentrations after exposure for 24 and 48 h. The significant changes of metabolites in ovaries of mussel exhibited the disturbances in energy metabolism and osmotic regulation, while in male samples triazophos only affected the energy metabolism. Moreover, glycine, sn-glycero-3-phosphocholine, ethanol, aspartate, etc. exhibited consistent variation tendency in both male and female individuals. While the changes of homarine, betaine, taurine, hypotaurine, malonate, β-alanine, succinate, and choline showed obviously gender-specific responses. Overall, this study confirmed the gender-specific responses in gonad of P. viridis to triazophos exposure.

Introduction

Triazophos, O,O-diethyl-1-H-1,2,4-triazo1-3-yl phosphorothioate, is a moderately toxic and broad-spectrum, non-systemic organophosphorus pesticide. It has been widely used in agriculture since the late 1970s in China, on various crops such as cotton, maize, paddy, and vegetable. In recent years, triazophos has been also intensively utilized as fungicide in intertidal aquaculture in China to protect farming shellfish such as Sinonovacula constricta and Tegillarca granosa from diseases. Due to the misuse of triazophos in intertidal aquiculture, fish and shrimp kill accidences caused by triazophos pollution took place sporadically in Fujian and Zhejiang coastal areas in China (Zhong et al., 2010). In addition, triazophos has been frequently detected in the coastal waters and aquatic products (Li et al., 2005, Xu et al., 2004). For instance, triazophos levels as high as 45.1 ng/L have been measured in the seawaters of Laizhou Bay (Wang et al., 2006). The widespread occurrence of triazophos in aquatic systems could represent a threat for aquatic species.

Traditional toxicological research has revealed that triazophos can induce diverse toxicities to aquatic species, including neurotoxicity, oxidative stress, and reproductive toxicity (Bao et al., 2010, Ge et al., 2011, Li and Tan, 2011, Li et al., 2013a, Li et al., 2013b, Xu et al., 2008, Xue et al., 2007). Bao et al. (2010) demonstrated that the transcripts of female Nilaparvata lugens vitellogenin were significantly up-regulated by triazophos treatment. Proteomic analysis detected some different proteins related to fecundity in female and male N. lugens respectively, after exposure to triazophos (Ge et al., 2011). Therefore, triazophos, as an endocrine disrupting chemical, is more likely to exhibit gender-specific toxic effect. In ecotoxicology, investigators do not often differentiate the male or female individuals when using mollusks as the experimental animal. But recent researches showed obviously variations in toxicological effects, when both male and female mussels were exposed by the same chemical (Ji et al., 2014a, Ji et al., 2014b). However, there is no report about gender-specific toxic effect of triazophos in marine mollusks so far.

The green-lipped mussel Perna viridis has been adopted as a biomonitor for assessing a wide range of chemical pollutants due to its high tolerance and accumulation of contaminants (Leung et al., 2014, Liu and Kueh, 2005). As a system biology approach, metabolomics, detecting all the low molecular weight metabolites (< 1000 Da) involved in all metabolic pathways in biological samples (Wu and Wang, 2010), has been widely used in environmental toxicology (Chen et al., 2016, Ji et al., 2013a, Ji et al., 2014a, Ji et al., 2014b, Ji et al., 2015, Ji et al., 2016, Song et al., 2016, Zhang et al., 2011a, Zhang et al., 2011b). In this work, metabolomics was applied to investigate the differential metabolic changes in male and female mussels after triazophos exposure. The resulting data may show metabolic biomarkers characterizing the toxicological effects of triazophos in P. viridis.