Comparative analysis on the photolysis kinetics of four neonicotinoid pesticides and their photo-induced toxicity to Vibrio Fischeri: Pathway and toxic mechanism

Highlights

• All the four neonicotinoids exhibit the photo-induced toxicity to V. fischeri, but with different toxic response.

• ROSs are involved in and play important roles in the photo-chemical transformation of intermediates.

• The amounts of ROSs play key roles in the photo-induced toxicity variation for the four neonicotinoids in different solution.

• A developed theoretical equation can well explain the toxicity variations of four neonicotinoids to V. fischeri.

Abstract

Neonicotinoids are widely used pesticides all over the world and pose severe water pollution. Although they can be degraded via absorbing sunlight, few attentions have been paid to the environmental risks of their photolysis products. In this paper, the photo-toxicity was investigated for four neonicotinoids (dinotefuran, nitenpyram, thiamethoxam and clothianidin) based on a series of experiments (i.e., photolysis kinetics, radical scavenging, bioluminescent inhibition test to Vibrio Fischeri and intermediate identification) and in-silico calculation of photolysis pathway. The results show that direct photolysis dominates the photolysis of the four neonicotinoids under simulated sunlight radiation. The bioluminescent inhibition kinetics shows that all four neonicotinoids have photo-induced toxicity to V. fischeri, but with different light-induced responses. Scavenging radicals (·OH and ¹O₂) will decrease the photo-induced toxicity of all the four neonicotinoids, indicating radicals play important roles to the photo-chemical reactions of intermediates. Dissolved organic matters exhibit slightly shading effect to the photolysis rates of four parent compounds. However, the ROSs generated by DOM can accelerate the photo-chemical reactions of intermediates, leading to different photo-induced toxicity in present of DOM. According to the detected intermediates and Gaussian calculations, there are different photolysis pathways and mechanisms for the four neonicotinoids. The calculation for photo-sensitization reactions with ³O₂ indicates that both energy transfer reactions and electron transfer reactions can be produced under simulated sunlight radiation, which further consolidate that reactive oxygen species are involved in the photolysis process. A theoretical model has been developed to explain the toxicity variations of four neonicotinoids in different aqueous conditions.

Introduction

Neonicotinoids are widely used in crop protection and insect control due to their broad-spectrum, high efficiency and low toxicity to mammals (Morrissey et al., 2015; Zhang et al., 2018a). They are currently the most extensively used insecticides in the world, representing a quarter of pesticide market (Jeschke et al., 2011; Wang et al., 2020). Due to the non-volatile and high water solubility, neonicotinoids have been frequently detected in soils and surfactant waters around the world (Hladik and Kolpin, 2016; Yi et al., 2019). It was reported that the maximum concentration of dinotefuran was 720 μg/L in the paddy water of Niigata Japan (Yokoyama et al., 2015). Their detection rates of thiamethoxam and clothianidin were 68.7% and 64.6%, respectively, from 48 sampling sites in the Danube river and the corresponding concentration ranges were 0.9–3.8 × 10⁻³ μg/L and 0.84–9.6 × 10⁻³ μg/L for the two neonicotinoids (Iancu et al., 2019). The concentration of nitenpyram could reach 1.25 μg/L in the drought period of Yangtze river (Chen et al., 2019a).

Neonicotinoids, such as dinotefuran, thiamethoxam and clothianidin, were unstable in aqueous environment when exposed to the sunlight (Lu et al., 2015; Kurwadkar et al., 2016). Nitenpyram is highly unstable under UV radiation (low pressure mercury lamp) and generates a number of products (Gonzalez-Marino et al., 2018). Because neonicotinoids can be degraded in surface runoff via photo-chemical transformation under solar radiation and their affinity to acetylcholinesterase in insects is much higher than that in mammals, these compounds were widely applied all over the world (Wang et al., 2020). However, according to recent researches, these insecticides may pose harmful effect to non-target organisms because some of the degradation products may pose more toxic effect than the parent compounds to aquatic organisms (e.g., fish, daphnia and green algae) (Gonzalez-Marino et al., 2018).

Assessment of the ecological risk for 60 agricultural chemicals revealed that more than 30% transformation products exhibited greater toxicity than their parent compounds (Sinclair and Boxall, 2003), and photo-chemical transformation is a major way of transformation in natural environment for these chemicals (El-Alawi et al., 2001; Challis et al., 2013). Spiramycin exhibited nontoxicity to Vibrio Fischeri (V. fischeri), but the toxicity increased if the sample was irradiated under simulated sunlight radiation due to the formation of some toxic photochemical transformation products (Calza et al., 2010). Some ozonization products of ketoprofen are more toxic than the original compound and pose greater effect to aquatic ecosystem (Zeng et al., 2018). Therefore, the risk assessment of a chemical should consider not only its parent compound, but also its intermediates or final products.

Photo-chemical transformation plays an important role in the transformation of neonicotinoids in the environment (Babenko et al., 2020). However, the detailed photolysis pathways are unclear for some neonicotinoids and the toxic mechanisms of photo-degraded neonicotinoids are still in blank stage (Kurwadkar et al., 2016; Aregahegn et al., 2018). Quantum chemistry method plays a key role in the understanding the photo-degradation pathway and toxic mechanism of organic compounds because it can simulate the whole process of the degradation (Hykrdova et al., 2018; Fan et al., 2020). It uses density functional theory (DFT) transition state model to assess the steric and energetic details of chemical reaction mechanisms (Qu et al., 2018; Townsend and Grayson, 2019). In this paper, V. fischeri, characterized by high sensitivity and convenient operation (5–30 min), was used as the model organism to investigate the photo-induced acute toxicity of four neonicotinoids (Parvez et al., 2006; Qu et al., 2016). Photolysis kinetics and photo-induced toxicity assays to V. fischeri were conducted under simulated sunlight radiation for four neonicotinoids. The concentrations of parent compounds and bioluminescent inhibition rates of test solutions were determined during photolysis period. At the same time, the photo-chemical transformation products were identified by liquid chromatography – tandem mass spectrometry with multiple reaction monitoring (LC-MS/MS). The objectives of this paper were: (1) To determine photo-induced toxicity of four neonicotinoids under simulated sunlight radiation; (2) To investigate the influence of reactive oxidation species (ROSs) over the photolysis and photo-induced toxicity; (3) To reveal the mechanism of photo-induced toxicity for four neonicotinoids. These analyses will advance understanding toxic mechanism of neonicotinoids to aquatic organisms and benefit the safety assessment of agricultural pollutants in aquatic environment.