Biodegradation of the neonicotinoid insecticide acetamiprid in surface water by the bacterium Variovorax boronicumulans CGMCC 4969 and its enzymatic mechanism

Sun, Shi-Lei; Yang, Wenlong; Guo, Jingjing; Zhou, Yi-Ning; Xue, Rui; Chen, Chen; Ge, Feng; Dai, Yinming

doi:10.1039/c7ra01501a

Cited by 44 publications

(47 citation statements)

References 39 publications

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“…The environmental fate of acetamiprid has attracted considerable attention, and microbial degradation is the key means for the dissipation of acetamiprid from the environment (15,16). In recent years, several microbial strains capable of degrading acetamiprid have been isolated, and the catabolic pathways of acetamiprid have been extensively studied (17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28). Four catabolic pathways of acetamiprid are illustrated in Fig.…”

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confidence: 99%

Pigmentiphaga sp. Strain D-2 Uses a Novel Amidase To Initiate the Catabolism of the Neonicotinoid Insecticide Acetamiprid

Yang

Wang

et al. 2020

Appl Environ Microbiol

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Acetamiprid, a chloronicotinyl neonicotinoid insecticide, is among the most commonly used insecticides worldwide, and its environmental fate has caused considerable concern. The compound 1-(6-chloropyridin-3-yl)-N-methylmethanamine (IM 1-4) has been reported to be the main intermediate during acetamiprid catabolism in microorganisms, honeybees, and spinach. However, the molecular mechanism underlying the hydrolysis of acetamiprid to IM 1-4 has not yet been elucidated. In this study, a novel amidase (AceAB) that initially hydrolyzes the C-N bond of acetamiprid to generate IM 1-4 was purified and characterized from the acetamiprid-degrading strain Pigmentiphaga sp. strain D-2. Based on peptide profiling of the purified AceAB and the draft genome sequence of strain D-2, aceA (372 bp) and aceB (2,295 bp), encoding the α and β subunits of AceAB, respectively, were cloned and found to be necessary for acetamiprid hydrolysis in strain D-2. The characteristics of AceAB were also systematically investigated. Though AceA and AceB showed 35% to 56% identity to the α and β subunits of the N,N-dimethylformamidase from Paracoccus aminophilus, AceAB was specific for the hydrolysis of acetamiprid and showed no activities to N,N-dimethylformamide or its structural analogs. IMPORTANCE Acetamiprid, among the top neonicotinoid insecticides used worldwide, is one of the most important commercial insecticides. Due to its extensive use, the environmental fate of acetamiprid, especially its microbial degradation, has caused considerable concern. Although the catabolic pathways of acetamiprid in microorganisms have been extensively studied, the molecular mechanisms underlying acetamiprid biodegradation (except for a nitrile hydratase) remain largely unknown, and the enzyme responsible for the biotransformation of acetamiprid into its main intermediate, IM 1-4, have not yet been elucidated. The amidase AceAB and its encoding genes, aceA and aceB, characterized in this study, were found to be necessary and specific for the initial hydrolysis of the C-N bond of acetamiprid to generate IM 1-4 in Pigmentiphaga sp. strain D-2. The finding of the novel amidase AceAB will greatly enhance our understanding of the microbial catabolism of the widely used insecticide acetamiprid at the molecular level.

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confidence: 99%

Pigmentiphaga sp. Strain D-2 Uses a Novel Amidase To Initiate the Catabolism of the Neonicotinoid Insecticide Acetamiprid

Yang

Wang

et al. 2020

Appl Environ Microbiol

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“…The molar transformation rate (the total amounts of IAM and IAA divided by the consumed amount of IAN) at 72 h was 86.6%, which indicated that the synthesis of IAM and IAA was the main pathway of IAN metabolism in strain CGMCC 4969. CGMCC 4969 NHase is a cobalt-dependent metalloenzyme, and adding cobalt ions apparently enhanced its activity (15,16). As Fig.…”

Section: Resultsmentioning

confidence: 85%

“…Characterization of V. boronicumulans CGMCC 4969 nitrile-converting enzymes. In V. boronicumulans CGMCC 4969, NHase activity for transforming IAN to IAM has been confirmed (16). The putative nitrilase-coding genes nitA and nitB and indoleacetamide hydrolase-coding genes iamA and iamB were overexpressed in E. coli Rosetta(DE3)/pLysS.…”

Section: Resultsmentioning

confidence: 90%

“…CGMCC 4969 NHase is a cobalt-type NHase, and it functions in the degradation of the neonicotinoid insecticides thiacloprid and acetamiprid (16). Amidases are classified into the amidase signature family and aliphatic amidases on the basis of their amino acid sequences (29).…”

Section: Resultsmentioning

confidence: 99%

“…They are also common plant symbionts found in the rhizosphere and used as model bacteria for the study of microbe-plant interactions (13,14). We previously isolated Variovorax boronicumulans strain CGMCC 4969, which can degrade the neonicotinoid insecticides thiacloprid and acetamiprid to their corresponding amide metabolites (15,16). V. boronicumulans CGMCC 4969 showed some plant growth-promoting traits, such as producing exopolymer substances, siderophores, ammonia, and hydrogen cyanide and secreting salicylate and 2, 3-dihydroxy benzoic acid (17).…”

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The Plant Growth-Promoting Rhizobacterium Variovorax boronicumulans CGMCC 4969 Regulates the Level of Indole-3-Acetic Acid Synthesized from Indole-3-Acetonitrile

Sun

Yang

Fang

et al. 2018

Appl Environ Microbiol

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is a metabolically diverse genus of plant growth-promoting rhizobacteria (PGPR) that engages in mutually beneficial interactions between plants and microbes. Unlike most PGPR, cannot synthesize the phytohormone indole-3-acetic acid (IAA) via tryptophan. However, we found that strain CGMCC 4969 can produce IAA using indole-3-acetonitrile (IAN) as the precursor. Thus, in the present study, the IAA synthesis mechanism of CGMCC 4969 was investigated. CGMCC 4969 metabolized IAN to IAA through both a nitrilase-dependent pathway and a nitrile hydratase (NHase) and amidase-dependent pathway. Cobalt enhanced the metabolic flux via the NHase/amidase, by which IAN was rapidly converted to indole-3-acetamide (IAM) and in turn to IAA. IAN stimulated metabolic flux via the nitrilase, by which IAN was rapidly converted to IAA. Subsequently, the IAA was degraded. CGMCC 4969 can use IAN as the sole carbon and nitrogen source for growth. Genome sequencing confirmed the IAA synthesis pathways. Gene cloning and overexpression in indicated that NitA has nitrilase activity and IamA has amidase activity to respectively transform IAN and IAM to IAA. Interestingly, NitA showed a close genetic relationship with the nitrilase of the phytopathogen Quantitative PCR analysis indicated that the NHase/amidase system is constitutively expressed, whereas the nitrilase is inducible. The present study helps our understanding of the versatile functions of nitrile-converting enzymes that mediate IAA synthesis and the interactions between plants and these bacteria. We demonstrated that CGMCC 4969 has two enzymatic systems-nitrilase and nitrile hydratase/amidase-that convert indole-3-acetonitrile (IAN) to the important plant hormone indole-3-acetic acid (IAA). The two IAA synthesis systems have very different regulatory mechanisms, affecting the IAA synthesis rate and duration. The nitrilase was induced by IAN, which was rapidly converted to IAA; subsequently, IAA was rapidly consumed for cell growth. The nitrile hydratase (NHase) and amidase system was constitutively expressed and slowly but continuously synthesized IAA. In addition to synthesizing IAA from IAN, CGMCC 4969 has a rapid IAA degradation system, which would be helpful for a host plant to eliminate redundant IAA. This study indicates that the plant growth-promoting rhizobacterium CGMCC 4969 has the potential to be used by host plants to regulate the IAA level.

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Role of Microbes in Degradation of Chemical Pesticides

Rana

Mardarveran

Gupta

et al. 2019

Microorganisms for Sustainability

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Biodegradation of the neonicotinoid insecticide acetamiprid in surface water by the bacterium Variovorax boronicumulans CGMCC 4969 and its enzymatic mechanism

Abstract: The plant growth-promoting rhizobacterium Variovorax boronicumulans CGMCC 4969 was used to degrade the neonicotinoid insecticide, acetamiprid (AAP), in surface water, and the enzymatic mechanisms of AAP degradation in V. boronicumulans CGMCC 4969 were explored. V. boronicumulans

Cited by 44 publications

References 39 publications

Pigmentiphaga sp. Strain D-2 Uses a Novel Amidase To Initiate the Catabolism of the Neonicotinoid Insecticide Acetamiprid

Pigmentiphaga sp. Strain D-2 Uses a Novel Amidase To Initiate the Catabolism of the Neonicotinoid Insecticide Acetamiprid

The Plant Growth-Promoting Rhizobacterium Variovorax boronicumulans CGMCC 4969 Regulates the Level of Indole-3-Acetic Acid Synthesized from Indole-3-Acetonitrile

Role of Microbes in Degradation of Chemical Pesticides

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