Background

Worldwide, the pesticides market is growing rapidly due to the increasing demand for food and high-yielding crops (Dhuldhaj et al. 2023). Neonicotinoids, often known as insecticides, are frequently employed to protect crops (such as wheat, rice, maize, soybeans, cotton, apple, sugar, beetroot, and potato) against a variety of pests and illnesses carried by insects, hence enhancing production (Simon-Delso et al. 2015; Katić et al. 2021). In order to enhance their insecticidal qualities, neonicotinoids are created and synthesized using the findings of investigations on the structure of nicotine (Humann-Guilleminot et al. 2019). Neonicotinoids, or synthetic nicotinoids with enhanced insecticidal qualities, include clothianidin, acetamiprid, dinotefuran, nitenpyram, imidacloprid, thiamethoxam, and thiacloprid, which have a structure similar to nicotine (Fig. 1). These chemicals are primarily used to control harmful pests, thereby safeguarding crops. They primarily target nicotinic acetylcholine receptors, which have endocrine-disrupting properties. Neonicotinoids, a family of insecticides, work by selectively binding to neuronal nicotinic acetylcholine receptors (nAChRs). This mechanism explains why these insecticides are effective, as they strongly activate insect nAChRs while having little affinity for vertebrate nAChRs. This characteristic reduces the risk of toxicity and enhances safety for non-target species. Although neonicotinoids are generally considered harmless, their presence in the environment can increase the risk of toxicity and exposure. Despite their low affinity for mammalian nAChRs, the abundance, diversity, and widespread presence of these receptors, along with their various functions, raise concerns about the potential impact of these pesticides on unintended species (Casida 2018). The mode of action of neonicotinoid and nicotinic acetylcholine receptor activity when (a) acetylcholine and (b) a neonicotinoid are present is illustrated in Fig. 2. Neonicotinoid environmental contaminants have skyrocketed during the last two decades as a result of their widespread use. Neonicotinoids have minimal soil adsorption (logKoc 1.4–2.3), high water solubility and minimal logKow (0.55–1.26). Partitioning properties and large consumption volume led to the pesticides prolonged persistence in soil as well as their enhanced leaching ability and transport via surface and subterranean runoff, which polluted both water and soil systems (Morrissey et al. 2015; Hladik et al. 2018; Gautam and Dubey 2022). The entry of neonicotinoids into the environment increases toxicological and hazardous pollutants, causing major health and environmental issues (Yu et al. 2020; Wu et al. 2021). Numerous studies have demonstrated the presence of persistent neonicotinoids in the environment, the detrimental effects of neonicotinoids on a variety of species, including mammals, and the potential routes of human exposure to neonicotinoids depicted in Fig. 3 (Cimino et al. 2017). Thus, it is critical to investigate operational and sustainable strategies for remediating polluted habitats caused by this pollutant (Gautam and Dubey 2023). Several methods have been developed to remove neonicotinoids and their leftovers from soil and water sources (Pang et al. 2020). Conventional physiochemical cleanup methods are difficult, costly and time-consuming.

Fig. 1
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Chemical structure of nictotine and neonicotinoids

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Fig. 2
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Mechanism of action of neonicotinoids and nicotinic acetylcholine receptor activity when a acetylcholine and b a neonicotinoid

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Fig. 3
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Neonicotinoid occurrence in the environment: sources, routes, and effects

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Generally, a variety of techniques can be used to reduce hazardous materials in the environment, such as physical adsorption and sophisticated oxidant processes (Ye et al. 2019). It is important to develop effective methods that are both cost-effective and environmentally friendly. In conclusion, microbial remediation techniques are a promising option for remediating neonicotinoids, both on-site and off-site, due to their low cost, minimal environmental impact, low risk of secondary contamination, and compatibility with other technologies (Li et al. 2020). Microorganisms, including bacteria, fungi, and microalgae, are used in the environmentally friendly process of biodegradation, which eliminates harmful substances from the environment (Bala et al. 2022). Microbial breakdown of neonicotinoids is considered to be the most effective and environmentally friendly on-site remediation process (Hamada et al. 2019). Microorganisms with the ability to degrade substances and survive in high-stress pesticide concentrations can be employed for the remediation of polluted environments, including toxic waste sites and hazardous areas (Rana et al. 2015; Bhatt et al. 2019). These microorganisms produce enzymes that break down xenobiotic compounds, such as agrochemicals, into less environmentally harmful molecules when exposed to moderate conditions like temperature, pH, medium, and salinity (Parte et al. 2017a, b).

Numerous microbes that can degrade neonicotinoids have been isolated and identified (Ahmad et al. 2021). In order to investigate the potential for biodegradation of neonicotinoids in polluted soil and water environments, a wide variety of microorganisms have been used (Hamada et al. 2019). However, further research is needed to understand the specific enzymes and genes involved in degradation. Currently, only a few studies have focused on the genetic and enzymatic basis of organisms that can degrade neonicotinoids, with the aim of developing more sustainable degradation methods (Parween et al. 2016). The main purpose of this review is to highlight the relevance, impact, and significant applications of microbial remediation and enzymatic techniques in efficiently eliminating harmful neonicotinoids from the environment.

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Microbial degradation of neonicotinoids

Numerous enzymes produced by microorganisms play a crucial role in the biotransformation and biodegradation processes involved in microbial remediation of non-engineering organic pollutants known as neonicotinoids (Anjos et al. 2021). Among these pollutants, imidacloprid and acetamiprid are extensively studied for microbial remediation due to their widespread use and commercialization. Research has shown that fungi, bacteria, and microalgae are capable of breaking down neonicotinoids, but bacteria are the most commonly studied organisms in this regard. Degradation rates for neonicotinoids by microbial consortia and isolated strains range from 20 to 100% (Wei et al. 2023). However, the chemical composition and properties of neonicotinoids, the specific strains of microorganisms employed, and the surrounding environment all significantly influence the degradation rates and pathways. Therefore, it is crucial to identify the specific strains capable of degrading particular neonicotinoids under specific conditions. The subsequent subsections will focus on the degradation of neonicotinoids by various microbes, including bacteria, fungi, and microalgae, and the utilization of their enzymes (Fig. 4).

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Neonicotinoids in environment and its bioremediation methods

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Bacterial biodegradation of neonicotinoids

Bacteria are excellent candidates for microbiological remediation of non-emergent organic pollutants due to their wide distribution and abundance in water and soil. In fact, more than forty bacterial strains have been identified as capable of degrading or modifying various neonicotinoids (Wei et al. 2023). Some commonly reported bacterial strains involved in efficient neonicotinoid removal include Acinetobacter, Ochrobactrum, Pseudomonas, Stenotrophomonas, Ensifer, Pseudoxanthomonas, Variovorax, Bacillus, and Partitioniphaga (Tang et al. 2012). Degradation rates of neonicotinoids can range from 24.2 to 100% depending on the initial concentrations (Wei et al. 2023). Figure 5 illustrates the biodegradation pathways of certain neonicotinoids (thiacloprid, acetamiprid, clothianidin, imidacloprid), while Table 1 provides more specific information on the microorganisms involved in neonicotinoid degradation and the characteristics that contribute to their effectiveness.

Fig. 5
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Biodegradation pathway of thiacloprid by Stenotrophomonas maltophilia CGMCC1.178, Pseudomonas sp. RPT 52 (Zhao et al. 2009; Gupta et al. 2016), Stenotrophomonas sp. cleave and hydrolyze the N-cyanoimine group of acetamiprid to create the metabolite N-methyl-(6-chloro-3-pyridyl)methylamine (Tang et al. 2012; Wang et al. 2013a, b), clothianidin using WRF Phlebia brevispora in conjunction with Enterobacter sp. TN3W-14 and Pseudomonas sp. TN3W-8, Ochrobactrum anthropi (Wang et al. 2019c; Harry-Asobara and Kamei 2019) aldehyde oxidase (nitro reduction of imidacloprid), by Pseudomonas sp. 1G, amidase (cleavage of N-cyanoimine group) using Pigmentiphaga sp. (bacterial strain) (Pandey et al. 2009; Yang et al. 2013)

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Table 1 Neonicotinoids biodegradation using bacterial strains
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Biodegradation of neonicotinoids by fungi

White-rot fungi (WRF) are highly effective organisms that have been widely utilized for the decomposition of various stubborn pollutants, including persistent organic pollutants (POPs), pesticides, endocrine disruptors, and dyes. Their efficient enzymatic activity and strong capability for external degradation are the reasons behind their success in this regard (Mir-Tutusaus et al. 2018). Studies conducted by Mir-Tutusaus et al. (2014) have demonstrated that Trametes versicolor (a type of WRF) can effectively break down agrochemicals such as carbofuran, imiprothrin, cypermethrin, and oxytetracycline, thereby reducing their toxic effects while maintaining cell viability. Moreover, WRFs have shown promising results in bioremediating soil and water contaminated with polychlorinated biphenyls (PCBs), petroleum, chlorophenol, polychlorinated dioxins, and polychlorinated dibenzo-p-furans (PCDD/Fs) (Anasonye et al. 2014; Shahi et al. 2016; Stella et al. 2017). Additionally, research has revealed that the white-rot fungus Phanerochaete sordida can degrade neonicotinoid pesticides such as nitenpyram, clothianidin, dinotefuran, and acetamiprid into compounds with minimal neurological toxicity (Mori et al. 2021). Therefore, the application of this ubiquitous white-rot fungus shows great promise in reducing the pollution caused by neonicotinoid pesticides.

Table 2 provides an overview of the degradation rates and durations of neonicotinoids by various fungi. The transformation ranges from 31% to complete degradation and takes place over a period of 5 days to 4 weeks. The white-rot fungi group, which includes Trametes versicolor, Phlebia brevispora, Phanerochaete sordida, and Phanerochaete chrysosporium, consists of the majority of fungal strains responsible for breaking down neonicotinoids.

Table 2 Neonicotinoids biodegradation using fungal strains
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Filamentous fungi known as “white-rot” are commonly found in decaying wood and can cause the wood to appear whitened (Yin et al. 2020; Zhuo and Fan 2021). These fungi possess a distinctive ligninolytic system, which includes extracellular enzymes such as laccase (Lac), lignin peroxidase (Lip), manganese peroxidase (MnP), and versatile peroxidase (VP). These enzymes are highly effective in breaking down a wide range of organic pollutants and exhibit low substrate specificity.

The fungal breakdown of neonicotinoids is primarily carried out by internal enzymes such as cytochrome P450 and peroxidase (POD), as well as extracellular enzymes like lignin peroxidase, manganese peroxidase, laccase, and apoenzymes produced by fungal mycelia. The metabolic mechanisms used by bacteria and fungi to break down neonicotinoids are similar. However, reports suggest that cytochrome P450 plays a more significant role in the breakdown of neonicotinoids by fungus. In the case of the commonly studied WRF, Phanerochaete chrysosporium, the inhibition of cytochrome P450 results in a slower degradation rate of acetamiprid (Wang et al. 2019a).

The main enzymes in P. chrysosporium that break down the chloropyridinyl group and target the side chains of acetamiprid, imidacloprid, and thiamethoxam through N-dealkylation are two cytochrome P450 isozymes: CYP5147A3 and CYP5037B3 (Mori et al. 2021). Most WRF strains convert neonicotinoids into metabolites that are either less toxic or non-toxic. However, certain modified products exhibit increased toxicity compared to the original substances. For example, Phanerochaete sordida YK-624 converted dinotefuran into a more hazardous metabolic by-product, while Trametes versicolor transformed imidacloprid and dinotefuran into hydroxylated derivatives with higher toxicity (Wang et al. 2019b; Hu et al. 2022). Harry-Asobara and Kamei (2019) proposed a potential method to enhance the decomposition of acetamiprid and clothianidin by using the WRF Phlebia brevispora in combination with Enterobacter sp. TN3W-14 and Pseudomonas sp. TN3W-8, two bacteria that promote mycelial morphology and proliferation. This approach utilizes a combination of high- and low-neonicotinoid metabolism fungi to effectively remediate neonicotinoids. Furthermore, there are only a few fungal strains currently capable of breaking down neonicotinoids (Table 2), and large-scale fermentation is time-consuming, making it challenging to employ these strains for industrial bioremediation purposes.

Biodegradation of neonicotinoids by microalgae

Aquatic creatures called microalgae are fast-developing and naturally found in various environments throughout the ocean, including freshwater and saltwater. These microalgae play a crucial role in maintaining the balance of the aquatic ecosystem as they are the foundation of the food pyramid (Goswami et al. 2022). Recent research has focused on the ability of microalgae to recover essential nutrients like nitrogen and phosphorus from secondary effluents, which helps prevent eutrophication and addresses environmental issues caused by certain pollutants (Nguyen et al. 2021; Abdelfattah et al. 2022; Mahari et al. 2022). Additionally, microalgae can be used for tertiary treatment in wastewater and produce biomass with various industrial applications (Salama et al. 2017). The biomass generated from microalgae growth can also serve as feedstock for industrial goods and be used in the commercial production of bioenergy. Microalgae have been successfully used to treat pesticides, dyes, heavy metals, and medications from sources like home wastewater, agricultural runoff, and pharmaceuticals (Ashour et al. 2021; Arutselvan et al. 2022; Bhatt et al. 2022). They are capable of degrading and detoxifying a wide range of organic and inorganic pollutants through bioadsorption, bioaccumulation, and biodegradation processes (Sutherland and Ralph 2019; Mustafa et al. 2021) (Table 3). These mechanisms offer promising approaches for removing pesticides at various points of entry. According to Nie et al. (2020), microorganisms can remove pesticides through metabolic processes.

Table 3 Biodegradation of neonicotinoids using microalgae
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Eukaryotic, photosynthetic microorganisms that are commonly found in aquatic environments are known as microalgae (Goswami et al. 2022). Removing xenobiotics from wastewater treatment plants has shown potential with them. In order for Nannochloropsis sp. to break down imidacloprid by around 50% in the first 20 h, Encarnação et al. (2021) state that light aeration and the presence of UV radiation were crucial. It has been proven possible to enhance imidacloprid elimination by mixing microalgae and bacteria in a biofilm reactor. In wastewater with visible light, Cheng et al. (2022a) demonstrated that the algae-bacteria biofilm reduced the toxicity of the wastewater and eliminated 74.9% of the inorganic particles. The steps involved in the breakdown process of imidazole include ring opening of imidazole and pyridine, hydrolysis, hydroxylation, and the loss of nitro and chlorine groups. Nevertheless, the mineralization was not complete. Nutrient recovery, carbon dioxide sequestration, and the removal of various pollutants, such as pesticides, endocrine disruptors, heavy metals, and medications, are among the multifunctional benefits of microalgae-mediated remediation (Sharma et al. 2022). Microalgae-mediated remediation may be used to complex pollution situations due to its versatility. To fully explore its potential to transform poisons into valuable items that will conserve resources, more study is necessary.

Enzyme-mediated degradation of neonicotinoids

Table 4 provides a summary of the most recent research on the enzymes that degrade imidacloprid. According to Pang et al. (2020), the ABC transporter, which facilitates the detoxification of foreign organisms also known as xenobiotic detoxification, is partly responsible for insects’ ability to detoxify pesticides. ABCG3, an anti-imidacloprid gene derived from Bemisia tabaci, is more highly expressed in females than in males. The suppression of ABCG3 mediated by RNA interference can significantly increase the mortality rate of adult Bemisia tabaci (He et al. 2019). 44 DcitABC transporters have been identified using the Diaphorina citri transcriptome and genome database. In addition to metabolic enzyme genes, DcitABC transporters are well characterized in several D. citri species and play a role in the detoxification of imidacloprid (Liu et al. 2020). Detoxification enzymes in insects, such as glutathione S-transferase, esterase, and P450s, are responsible for catabolizing toxins and pesticides. These enzymes have the ability to increase the gene copy number, mRNA levels, and coding sequence variety by introducing point mutations in the targeted pesticide gene (Li et al. 2007). One well-known family of monooxygenases is cytochrome P450, which has been recognized for its capability to utilize molecular oxygen for substrate oxidation and hydroxylation. This family of enzymes shows promises in various industrial processes (Scott et al. 2008). Cytochrome P450 enzymes are involved in multiple processes, including the metabolism and biosynthesis of foreign substances. Studies have revealed that insects possess a wide range of P450 genes, ranging from 46 to over 150, and each gene may encode a distinct P450 enzyme.

Table 4 Microbial enzymes in neonicotinoids biodegradation
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Bioinformatics analysis has demonstrated that BtCPR is a transmembrane protein. With a molecular weight of 76.73 kDa, it consists of NADPH, FAD, and FMN, three conserved binding domains. The highest concentrations of BtCPR are found in the tissues of the adult male whitefly’s head. Its sensitivity to imidacloprid is significantly increased when BtCPR is inhibited (He et al. 2020). Furthermore, Nilaparvata lugens does not show imidacloprid and pyrazine cross-resistance. Nilaparvata lugens has the potential to develop resistance to imidacloprid due to the efficient metabolism of the drug by two P450s, CYP6AY1 and CYP6ER1 (Yang et al. 2016). In the Chinese lizard Eremias argus, CYP2C9 and aldehyde oxidase play a significant role in the reduction of nitro groups, whereas CYP3A4 controls the hydroxylation and desaturation processes (Raby et al. 2018).

Microbial degradation mechanism of neonicotinoids

The microbial breakdown of neonicotinoids is primarily carried out by metabolic processes. These processes involve a specific chemical group called the “magic nitro group.” This group consists of a nitrile group (–C≡N) for acetamiprid and thiamethoxam, and a nitro group (=N–NO2) for imidacloprid, clothianidin, thiamethoxam, nitenpyram, and dinotefuran. The breakdown process begins with the transformation of the nitro group, which can be achieved through denitration, nitro reduction, cleavage, and hydrolysis of the N-cyanoimine group. Subsequent metabolic reactions include dichlorination, hydrolysis, ring opening, oxidation or reduction, and oxidative or reductive cleavage. Throughout the early and middle stages of degradation, various responses can occur. Gautam and Pandey (2022) have identified two bacterial strains, Sphingobacterium sp. and Agrobacterium sp., capable of degrading imidacloprid in pesticide-contaminated farming soils. These strains have the ability to modify imidacloprid, reducing its lethality by lowering the nitro group and producing a less harmful imidacloprid guanidine compound. The metabolic pathways of other neonicotinoids, including imidacloprid, have also been studied.

According to Tang et al. (2012), Stenotrophomonas sp. can cleave and hydrolyze the N-cyanoimine group of acetamiprid, resulting in the formation of the metabolite N-methyl-(6-chloro-3-pyridyl)methylamine. Similarly, Wang et al. (2013a) also observed that Pigmentiphaga sp. AAP-1 produces the same metabolic product (N-methyl-(6-chloro-3-pyridyl)methylamine) by hydrolyzing and cleaving the N-cyanoimine group of acetamiprid. This particular metabolite is considered to be minimally harmful to bees and mammals. In another study, Zhou et al. (2013) found that the bacterial strain Ensifer adhaerens TMX-23 transforms the N-nitroimino group of thiamethoxam into urea and N-nitrosoimine. Furthermore, Sharma et al. (2014) conducted a comprehensive study on the metabolism of imidacloprid using Bacillus alkalinitrilicus obtained from sugarcane cultivation soil. Their study revealed three metabolic products: 6-chloronicotinic acid, guanidine imidacloprid, and nitroso imidacloprid. These results suggest the presence of two different metabolic pathways. In the first pathway, imidacloprid is reduced to nitroso imidacloprid and guanidine imidacloprid, while in the second pathway, it is oxidized to 6-chloronicotinic acid. Both pathways involve the conversion of intermediates into CO2.

In a study conducted by Shettigar et al. (2012), it was discovered that the bacterial strain Bradyrhizobiaceae SG-6C has the ability to convert 6-chloronicotinic acid to CO2, despite being identified in previous studies as a dead-end metabolite (DEM) of imidacloprid and acetamiprid breakdown. This finding suggests a potential method for fully degrading neonicotinoids. Neonicotinoids, such as imidacloprid and thiamethoxam, rely on hydroxylation for their metabolism, with the resulting metabolites exhibiting varying levels of toxicity. Stenotrophomonas maltophilia CGMCC 1.1788 was found to hydroxylate both imidacloprid and thiamethoxam, but Zhao et al. (2009) discovered that the metabolic products of imidacloprid (5-hydroxy and olefin imidacloprid) were more toxic than the parent molecule, while the metabolic compounds of thiamethoxam (4-hydroxy thiamethoxam and the resulting 4-ketone thiamethoxam imine) were less toxic. Despite a limited number of studies proposing enzymatic and genetic mechanisms, as well as metabolic pathways, for the microbial degradation of neonicotinoids, it has been demonstrated that a variety of bacterial enzymes are involved in different metabolic activities. Aldehyde oxidase, carried out by Pseudomonas sp. 1G, is responsible for the nitro reduction of imidacloprid, while Pigmentiphaga sp. utilizes amidase to cleave the N-cyanoimine group of acetamiprid. Nitrile hydratase (NHase) and cytochrome P450 are two other enzymes that assist in the degradation of neonicotinoids (Pandey et al. 2009; Yang et al. 2013). NHase and cytochrome P450 are known to play a significant role in breaking down specific neonicotinoids. Various species have demonstrated that cytochrome P450 enzymes actively facilitate the degradation of neonicotinoids. Research has shown a close connection between hydroxylation and P450 in bacteria. For example, in a study conducted by Guo et al. (2020) using Hymenobacter latericoloratus CGMCC 16346 to reduce imidacloprid levels in surface water, it was found that piperonyl butoxide, a suppressor of cytochrome P450 monooxygenase, hindered the removal of imidacloprid hydroxyl group, resulting in the formation of 5-hydroxy and olefin imidacloprid. Additionally, NHase plays a crucial role in the mineralization of two neonicotinoids, acetamiprid and thiamethoxam, by catalyzing the synthesis of amides from nitriles. NHase can aid in the reaction of acetamiprid hydration to (E)-N2-carbamoyl-N1-[(6-chloro-3-pridyl)methyl]. A number of bacteria, such as Pseudaminobacter salicylatoxidans CGMCC and Variovorax boronicumulans CGMCC 4969 1.17248, require N1-methylacetamidine (IM-1-2) in order to break down acetamiprid (Sun et al. 2017; Guo et al. 2021).

Conclusions

The previous sections provided an overview of neonicotinoids, which are commonly used insecticides in agriculture due to their strong insecticidal properties. Neonicotinoids target the nicotinic acetylcholine receptors (nAChRs) in insects neurons, specifically activating them without affecting vertebrates. However, there is still a possibility of toxicity and exposure to neonicotinoids in the environment. Although these insecticides have a reduced affinity for mammalian nAChRs, the abundance and distribution of these receptors raise concerns. Therefore, it is crucial to consider the long-term negative impacts of neonicotinoids on the environment and work toward removing these residues from polluted ecosystems. Using efficient neonicotinoid-degrading bacteria for remediation is considered a viable approach in contaminated areas. The microbial degradation processes and toxicity of specific neonicotinoids have been extensively studied, while others have received less attention. Many breakdown intermediates of neonicotinoid pesticides, especially imidacloprid, pose a greater risk than the original compound.

The researchers studied microorganisms found in wastewater, rhizosphere soils, neonicotinoid-polluted agricultural soils, and microbial preservation centers. None of the isolated bacteria were able to completely metabolize thiacloprid, acetamiprid, imidacloprid, clothianidin, and thiamethoxam. However, different bacteria were found to break down imidacloprid and acetamiprid simultaneously, producing carbon dioxide and water. The long-term effectiveness of imidacloprid and other neonicotinoids in causing environmental degradation depends on the isolation or cultivation of such bacteria. Only a limited number of studies have determined the enzymes and breakdown pathways involved. Further research is needed to understand the process of bioremediation through the breakdown of microorganisms and enzymes in order to develop an organized approach to treating neonicotinoids.

In order to comprehend the degradation processes in a polluted environment, it is crucial to examine how genes and enzymes function. Different microorganisms that can break down neonicotinoid compounds have been found, but research on the enzymes and functional genes of these species has been limited. Therefore, before extensively utilizing neonicotinoid-degrading microorganisms for bioremediation, a significant amount of fundamental research is needed. High-throughput sequencing techniques have been proposed as a potential tool for thoroughly annotating the genes and metabolites generated during microbial breakdown.

Moreover, the development of modified degrading microbes and the utilization of degrading genes and enzymes are necessary. Additionally, it is important to examine whether the collaborative breakdown of microbial consortia helps prevent the accumulation of hazardous compounds. Recent advancements in omics-based technologies have provided new insights into pesticide biodegradation, which could contribute to the formulation of an effective bioremediation strategy for neonicotinoid-polluted environments.