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Insights Into the Toxicity and Degradation Mechanisms of Imidacloprid Via Physicochemical and Microbial Approaches

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Insights Into the Toxicity and Degradation Mechanisms of Imidacloprid Via Physicochemical and Microbial Approaches toxics Review Insights into the Toxicity and Degradation Mechanisms of Imidacloprid Via Physicochemical and Microbial Approaches Shimei Pang 1,2, Ziqiu Lin 1,2, Yuming Zhang 1,2, Wenping Zhang 1,2, Nasser Alansary 1,2, Sandhya Mishra 1,2 , Pankaj Bhatt 1,2 and Shaohua Chen 1,2,* 1 State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou 510642, China; [email protected] (S.P.); [email protected] (Z.L.); [email protected] (Y.Z.); [email protected] (W.Z.); [email protected] (N.A.); [email protected] (S.M.); [email protected] (P.B.) 2 Guangdong Laboratory for Lingnan Modern Agriculture, Guangzhou 510642, China * Correspondence: [email protected]; Tel.: +86-20-8528-8229 Received: 22 July 2020; Accepted: 26 August 2020; Published: 1 September 2020 Abstract: Imidacloprid is a neonicotinoid insecticide that has been widely used to control insect pests in agricultural fields for decades. It shows insecticidal activity mainly by blocking the normal conduction of the central nervous system in insects. However, in recent years, imidacloprid has been reported to be an emerging contaminant in all parts of the world, and has different toxic effects on a variety of non-target organisms, including human beings, due to its large-scale use. Hence, the removal of imidacloprid from the ecosystem has received widespread attention. Different remediation approaches have been studied to eliminate imidacloprid residues from the environment, such as oxidation, hydrolysis, adsorption, ultrasound, illumination, and biodegradation. In nature, microbial degradation is one of the most important processes controlling the fate of and transformation from imidacloprid use, and from an environmental point of view, it is the most promising means, as it is the most effective, least hazardous, and most environmentally friendly. To date, several imidacloprid-degrading microbes, including Bacillus, Pseudoxanthomonas, Mycobacterium, Rhizobium, Rhodococcus, and Stenotrophomonas, have been characterized for biodegradation. In addition, previous studies have found that many insects and microorganisms have developed resistance genes to and degradation enzymes of imidacloprid. Furthermore, the metabolites and degradation pathways of imidacloprid have been reported. However, reviews of the toxicity and degradation mechanisms of imidacloprid are rare. In this review, the toxicity and degradation mechanisms of imidacloprid are summarized in order to provide a theoretical and practical basis for the remediation of imidacloprid-contaminated environments. Keywords: imidacloprid; toxicity; microbialdegradation; physicochemicaldegradation; degradationmechanisms 1. Introduction Imidacloprid (1-((6-chloro-3-pyridinyl) methyl)-N-nitro-2-imidazolidnimine) is a colorless crystal neonicotinoid insecticide, which belongs to the chloronitroguanidine compounds, with a melting point of 143.8 ◦C. Imidacloprid is a polar compound, chemically stable under neutral and acidic conditions, but decomposes gradually in alkaline solutions [1]. Systemic insecticide neonicotinoids are recognized as a valuable tool for pest control, especially imidacloprid. It is widely used to control pests with piercing–sucking mouthparts on crops. In addition, it is reported that imidacloprid can effectively cure many cases of cardiopulmonary parasite infection in European feral cats [2]. Toxics 2020, 8, 0065; doi:10.3390/toxics8030065 www.mdpi.com/journal/toxics Toxics 2020, 8, x FOR PEER REVIEW 2 of 35 melting point of 143.8 °C. Imidacloprid is a polar compound, chemically stable under neutral and acidic conditions, but decomposes gradually in alkaline solutions [1]. Systemic insecticide Toxicsneonicotinoids2020, 8, 0065 are recognized as a valuable tool for pest control, especially imidacloprid. It is widely2 of 31 used to control pests with piercing–sucking mouthparts on crops. In addition, it is reported that imidacloprid can effectively cure many cases of cardiopulmonary parasite infection in European feral catsImidacloprid [2]. Imidacloprid was first registeredwas first registered in the United in the States United (U.S.) States in 1992 (U.S.) by Milesin 1992 Inc., by and Miles was Inc., approved and was by approvedthe U.S. Environmental by the U.S. Environmental Protection Agency Protection (EPA) inAgency 1994 [1 (EPA)]. Although in 1994 imidacloprid [1]. Although was imidacloprid listed as one wasof the listed world’s as one best-selling of the world’s pesticides best-selling in 2000, pesticides the European in 2000, Union the European banned itsUnion use onbanned outdoor its use crops on outdoorentirely incrops 2018, entirely after suspending in 2018, after its suspending use in 2013 its [3]. use Imidacloprid in 2013 [3]. canImidacloprid be used for can leaf be spraying used for andleaf sprayingsoil and seed and treatment,soil and seed all treatment, of which have all of had whic negativeh have ehadffects negative on ecosystem effects services,on ecosystem including services, the includingkilling of non-targetthe killing organisms of non-target with organisms significant with economic significant value, economic such as pollinators, value, such honey as pollinators, providers, honeyand natural providers, insects and that natural benefit insects farmers that [4 ].benefit The pesticidefarmers [4]. toxicity The pesticide load on thetoxicity environment load on hasthe environmentincreased approximately has increased 50 approximately times in the past 50 20 times years. in Thethe negativepast 20 years. influence The onnegative related influence ecosystems on relatedis the main ecosystems cause ofis the main increase cause in of the the toxicity increase load, in the which toxicity in turnload, may which be in a turn threat may to be the a healththreat toof beesthe health and other of bees pollinators, and other resulting pollinators, in a resulting reduction in in a beneficialreduction insectin beneficial populations, insect otherpopulations, insects, otherand insect-eating insects, and birds insect-eating [5]. Imidacloprid birds [5]. damages Imidacloprid the biological damages nervous the biological system throughnervous calciumsystem throughion imbalance, calcium mitochondrial ion imbalance, dysfunction, mitochondrial oxidative dysfunction, stress, and oxidative DNA damage, stress, ultimatelyand DNA leading damage, to ultimatelybiological deathleading [6 ].to In biological recent years, death imidacloprid [6]. In recent has years, been imidacloprid reported to be has an been emerging reported contaminant to be an emergingin all parts contaminant of the world, in and all it parts has the of potentialthe world, to adverselyand it has impact the potential ecosystems to andadversely human impact health (Figureecosystems1). Therefore, and human the health removal (Figure of imidacloprid 1). Therefore, residues the removal from the of ecosystem imidacloprid is a worldwide residues from concern the ecosystemand priority. is a worldwide concern and priority. Figure 1. TheThe fate fate and occurrence of imid imidaclopridacloprid in the environment. In nature, (bio) degradation is one of the most important processes controlling the fate of and transformation from imidacloprid use. There There are are many many aspects of pesticide degradation research worldwide [7[7–10].–10]. The The current current main main methods methods of imidacloprid of imidacloprid degradation degradation include: include: (1) Physical (1) methodsPhysical methodssuch as ultrasonic such as ultrasonic technology, technology, washing, absorption, washing, andabsorption, ionizing and radiation; ionizing (2) radiation; chemical methods (2) chemical such methodsas hydrolysis, such oxidativeas hydrolysis, decomposition, oxidative anddecomposi light chemicaltion, and degradation; light chemical and (3)degradation; biological methodsand (3) biologicalsuch as microbial methods degradation such as microb enzymesial degradation and engineering enzymes bacteria and engin (Figureeering2). These bacteria degradation-related (Figure 2). These studies have made considerable progress. Facing the persistence of surface water and the high leaching potential of groundwater, many traditional methods, such as Fenton oxidation, photodegradation, catalytic oxidation, adsorption, and biodegradation, are being used to deal with these problems [1]. Toxics 2020, 8, x FOR PEER REVIEW 3 of 35 degradation-related studies have made considerable progress. Facing the persistence of surface water and the high leaching potential of groundwater, many traditional methods, such as Fenton oxidation, Toxicsphotodegradation,2020, 8, 0065 catalytic oxidation, adsorption, and biodegradation, are being used to deal3 with of 31 these problems [1]. Figure 2. Degradation methods of imidacloprid. Figure 2. Degradation methods of imidacloprid. The effects and fate of pesticides on soil depend, in part, on farming practices [11]. Pesticide residues in theThe soil effects are aff ectedand fate by the of applicationpesticides on of fertilizer,soil depend, its pH in value,part, on the farming soil type, practices and the surface[11]. Pesticide [12–15]. Underresidues natural in the conditions, soil are affected imidacloprid by the in applicatio soil or watern of canfertilizer, be degraded its pH by value, microorganisms the soil type, or throughand
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