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Sulfoxaflor Degraded by Aminobacter Sp. CGMCC 1.17253 Through

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Sulfoxaflor Degraded by Aminobacter Sp. CGMCC 1.17253 Through pubs.acs.org/JAFC Article Sulfoxaflor Degraded by Aminobacter sp. CGMCC 1.17253 through Hydration Pathway Mediated by Nitrile Hydratase Wen-Long Yang, Zhi-Ling Dai, Xi Cheng, Ling Guo, Zhi-Xia Fan, Feng Ge,* and Yi-Jun Dai* Cite This: J. Agric. Food Chem. 2020, 68, 4579−4587 Read Online ACCESS Metrics & More Article Recommendations *sı Supporting Information ABSTRACT: Sulfoxaflor, a sulfoximine insecticide, could efficiently control many insect pests of sap-feeding. Microbial degradation of sulfoxaflor and the enzymatic mechanism involved have not been studied to date. A bacterial isolate JW2 that transforms sulfoxaflor to X11719474 was isolated and identified as Aminobacter sp. CGMCC 1.17253. Both the recombinant Escherichia coli strain harboring the Aminobacter sp. CGMCC 1.17253 nitrile hydratase (NHase) gene and the pure NHase acquired sulfoxaflor- degrading ability. Aminobacter sp. CGMCC 1.17253 NHase is a typical cobalt-containing NHase content of subunit α, subunit β, and an accessory protein, and the three-dimensional homology model of NHase was built. Substrate specificity tests showed that NHase catalyzed the conversion of acetamiprid, thiacloprid, indolyl-3-acetonitrile, 3-cyanopyridine, and benzonitrile into their corresponding amides, indicating its broad substrate specificity. This is the first report of the pure bacteria degradation of the sulfoxaflor residual in the environment and reveals the enzymatic mechanism mediated by Aminobacter sp. CGMCC 1.17253. KEYWORDS: insecticide, biodegradation, Aminobacter sp. CGMCC 1.17253, sulfoxaflor, nitrile hydratase ■ INTRODUCTION 3-yl]ethanol}, X11719474 [N-(methyl(oxido){1-[6- fl fl (trifluoromethyl)pyridin-3-yl]ethyl}-k4-sulfanylidene)urea], Sulfoxa or (SUL, X14422208, [N-[methyloxido[1-[6-(tri uor- fl omethyl)-3-pyridinyl] ethyl]-λ4-sulfanylidene] cyanamide]) is X11519540 {[5-(1-methylsulfonyl)ethyl]-2-(tri uoromethyl)- pyridine}, X11579457 ({5-[1-(S-methylsulfonimidoyl)ethyl]}- a novel sulfoximine insecticide. At the core of its structure, fl fl there are a 2-CF -pyridine fragment and a distinctive N- 2-(tri uoromethyl)pyridine), and 5-ethyl-2-(tri uoromethyl)- 3 pyridine, could be detected in the environment, thereby cyanosulfoximine moiety. Similar to the target site of presenting an environmental problem (Figure 1A).5,13,14 To neonicotinoids, nicotinic acetylcholine receptors (nAChRs) achieve successful integrated pest management in protected of insects are the target site of sulfoxaflor, and sulfoxaflor could 1 crops, the first evaluation of the compatibility with pesticides efficiently control many insect pests of sap-feeding. Sulfoxaflor and other nontarget organisms is required. However, despite has been used in the control of many pests such as Aphis the lack of cross-resistance between neonicotinoids, there are gossypii Glover, Philaenus spumarius, and Laodelphax striatel- 2−4 still reports that sulfoxaflor exerts toxicity against many non- lus as well as numerous crops such as brown rice and 5,6 target organisms, such as earthworms, bumblebees, and lettuce. − Amblyseius swirskii.15 17 Furthermore, reports that sulfoxaflor Downloaded via NANJING NORMAL UNIV on April 23, 2020 at 02:38:16 (UTC). Sap-feeding insects cause considerable economic losses in residues exert toxicity in rats and mice, as animal models of terms of crop damage and several classes of insecticides have ff human disease, are of great concern. In rats, high-dose dietary been used to e ectively control many pests of sap-feeding. The fl See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles. exposure to sulfoxa or in the gestational period caused most commonly used insecticides in the world are reduced neonatal survival and fetal abnormalities (primarily neonicotinoids. However, there is increasing evidence that limb contractures).18 High dietary doses of sulfoxaflor induced neonicotinoids are poisonous to pollinators as well as other 19 − rodent hepatotoxicity in mice. Sulfoxaflor in the environ- nontarget organisms, such as wild bees and honeybees.7 9 It ment, therefore, presents a serious health threat. has led to several countries banning the usage of neonicotinoid Many insecticide residues are degraded by microorganisms insecticides, there for developing alternative pest control and therefore considered of moderate risk to the environ- products is necessary.10 Sulfoxaflor could effectively control ment.20,21 Many neonicotinoids insecticide environmental lots species of sap-feeding insects but lacks cross-resistance residual removed by microorganisms has been studied. with neonicotinoids; consequently, it is regarded as a potential Neonicotinoids insecticide imidacloprid could be degraded successor to neonicotinoid insecticides.11 However, despite being highly effective against sap-feeding insects, showing decreased toxicity compared with other Received: October 23, 2019 insecticides and lacking cross-resistance with neonicotinoids, Revised: January 31, 2020 sulfoxaflor residues remained detectable in brown rice, rice Accepted: March 31, 2020 straw, and paddy field water after field application.5,12 Published: March 31, 2020 Sulfoxaflor and its metabolites, X11596066 (5-ethyl-2-trifluor- omethylpyridine), X11721061 {1-[6-(trifluoromethyl)pyridin- © 2020 American Chemical Society https://dx.doi.org/10.1021/acs.jafc.9b06668 4579 J. Agric. Food Chem. 2020, 68, 4579−4587 Journal of Agricultural and Food Chemistry pubs.acs.org/JAFC Article Figure 1. Metabolic pathways of sulfoxaflor and the molecular structures of the substrates used for specificity testing. (A) Various pathways for the metabolism of sulfoxaflor. (B) Molecular structures of the NHase substrates used for specificity testing. by Pseudomonas putida KT2440 through oxidation pathway of a novel bacteria-based method for sulfoxaflor bioremedia- into 5-hydroxy and olefin imidacloprid derivatives, and it also tion. could be degraded through nitroreduction pathway into nitroso, guanidine, and urea imidacloprid derivatives.22 ■ MATERIALS AND METHODS Neonicotinoid insecticide thiacloprid could be degraded into Chemicals and Media. Sulfoxaflor was purchased from Hubei thiacloprid amide by Ensifer meliloti CGMCC 7333 through Zhengxingyuan Fine Chemical Co. (Wuhan, China) and had a purity 21 of 95%. Other reagents were purchased from Sinopharm Chemical hydrolysis pathway. Neonicotinoid insecticide acetamiprid Reagent Co. (Shanghai, China) and were of analytical grade. could be degraded into (E)-1-(1-(((6-chloropyridin-3-yl)- Acetonitrile was of high-performance liquid chromatography methyl)(methyl)amino)ethylidene)urea by Streptomyces canus (HPLC) grade and purchased from Tedia Co. (Fairfield, OH). The 20 CGMCC 13662 through hydrolysis pathway.23 However, pure formula of mineral salt medium (MSM) was described previously. isolate of microbial degradation of sulfoxaflor has not been The lysogeny broth (LB) comprised of 10 g of NaCl, 10 g of tryptone, and 5 g of yeast extract and dissolved in 1 L of deionized water (pH reported before. 7.2). The LB agar medium had the same formula as that of LB but 2% This study aimed to isolate sulfoxaflor-degrading micro- agar was added. organisms out of soil source. Subsequently, the metabolic X11719474 was prepared as follows: sulfoxaflor was transformed by pathways as well as enzymes required for sulfoxaflor Escherichia coli Rosetta (DE3) resting cells overexpressing Amino- bacter sp. CGMCC 1.17253 NHase (see the Cloning of the biodegradation were characterized. The findings of this study fl Aminobacter sp. CGMCC 1.17253 NHase Gene in E. coli Rosetta will enhance the understanding of sulfoxa or degraded by (DE3) section). NHase was induced to express in the recombinant E. microbes in the environment and may aid in the development coli Rosetta (DE3) strains in 600 mL of LB following the method 4580 https://dx.doi.org/10.1021/acs.jafc.9b06668 J. Agric. Food Chem. 2020, 68, 4579−4587 Journal of Agricultural and Food Chemistry pubs.acs.org/JAFC Article described in the Overexpression of Aminobacter sp. CGMCC High-Performance Liquid Chromatography (HPLC) Anal- 1.17253 NHase and Enzymatic Activity Assay section. Five hundred yses Method. To analyze sulfoxaflor and its metabolites, an HC-C18 milligrams per liter sulfoxaflor solution (dissolve in 50 mmol/L column (4.6 mm × 250 mm, 5 μm; Agilent, Santa Clara, CA) phosphate-buffered saline (PBS), pH 7.0) was transformed by E. coli mounted on an Agilent 1200 HPLC system was used. The flow rate of Rosetta (DE3) resting cells overexpressing Aminobacter sp. CGMCC elution was 1 mL/min. The mobile phase was water (containing 1.17253 NHase following the method described in the Isolation and 0.01% acetic acid) and acetonitrile, and the ratio of water (containing Identification of Sulfoxaflor-Degrading Bacterial Strain JW2 section 0.01% acetic acid) to acetonitrile was 70:30. The wavelength of the until sulfoxaflor had been thoroughly transformed. To remove the Agilent G1314A UV detector was 220 nm. cells, the transformation broth containing X11719474 was centrifuged Liquid Chromatography−Mass Spectrometry (LC−MS) − fi at 8000×g, 5 min. Then, the supernatant was collected and dried to a Analyses. An Agilent LC MS system (1290 In nity LC/6460 powder by freeze-drying. The powder was then extracted by ethyl Triple Quad MS; Agilent, Santa Clara, CA) in tandem with an acetate. Then, the ethyl acetate extraction contained X11719474 was electrospray ion source used in both positive- and negative-ion modes fi μ fi were used to analyze the sulfoxaflor-transformed sample by JW2 to concentrated
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