Rapid degradation of dimethomorph in polluted water and soil by Bacillus cereus WL08 immobilized on bamboo charcoal–sodium alginate

https://doi.org/10.1016/j.jhazmat.2020.122806Get rights and content

Highlights

  • Bacterium Bacillus cereus WL08 was the novel pure strain of dimethomorph-degrading.

  • Strain WL08 efficiently degraded dimethomorph to simple products.

  • Immobilization significantly improved tolerance and stability of WL08.

  • Immobilized WL08 rapidly degraded dimethomorph in water and soil.

  • This study provides a feasible microbe-based strategy for dimethomorph remediation.

Abstract

The presence of hazardous dimethomorph residues in the environment poses a threat to birds, aquatic organisms and mammals. The novel pure strain Bacillus cereus WL08 responsible for detoxifying dimethomorph was isolated from dimethomorph-polluted soils. The immobilized system of WL08 was developed using bamboo charcoal (BC) and sodium alginate (SA). Immobilization significantly improved tolerance and stability of strain WL08. Under optimal conditions of pH 7.0 and 30 ℃, free and immobilized WL08 degraded 66.95% and 96.88% of 50 mg/L dimethomorph within 72 h, respectively. Moreover, strain WL08 effectively degraded dimethomorph to simple products which were lower toxic than dimethomorph. In a continuous reactor system, immobilized WL08 removed 85.61% of dimethomorph for 30 d at an influent concentration of 50–100 mg/L. In the field soil sprayed with 4.20 kg a.i./ha 80% dimethomorph water dispersible granule (WDG) was treated by immobilized WL08, the lower half-life (1.93 d) was observed, as compared with free WL08 (4.28 d) and natural dissipation (23.82 d). Immobilized WL08 can be considered as a tool for the removal of dimethomorph in water–soil systems. This study provides a feasible microbe-based strategy for bioremediation of dimethomorph-polluted environments.

Introduction

Dimethomorph (4-[3-(4-chlorophenyl)-3-(3-4-dimethox-yphenyl) acryloyl] morpholine) is a selective-activity fungicide globally used to control downy mildews, crown and root rots, and late blights in many crops (Hengel and Shibamoto, 2003). Despite its benefits to agriculture, increasing evidences have confirmed that dimethomorph residues were detected in surface and ground waters, soils and agricultural products and its concentration values ranged from ng/L (ng/kg) to mg/L (mg/kg), these levels could pose risk to birds, aquatic organisms and mammals due to its hazardous nature of toxic residues (EPA (Environmental Protection Agency), 1998; Megateli et al., 2013; Avetta et al., 2014). For instance, Oliveira et al. (2013) found that dimethomorph had toxicity to some living organisms including soil and water microflora even at very low concentrations. Lunn (2007) and Teather et al. (2001) reported that dimethomorph possessed highly or moderate toxicity to fish and invertebrates. Megateli et al. (2013) and Dosnon-Olette et al. (2009, 2010) indicated that it had low toxicity towards some duckweed species. Cycon et al. (2010) and Wang et al. (2017) still demonstrated that dimethomorph might disturb some soil-inhabiting organisms (e.g. earthworms). Moreover, dimethomorph is extreme resistant to hydrolysis and has a quite long half-life in the ecosystem (Teather et al., 2001; Liang et al., 2011; Liu et al., 2012a).

The cost-effective and eco-friendly remediation strategy of dimethomorph-polluted water and soil systems is therefore essential to remove an ecological risk caused by hazardous dimethomorph residues. It has been reported that the duckweed Lemna minor and Spirodela polyrhiza could eliminate 41 and 26 μg/L dimethomorph from polluted wastewater, respectively (Dosnon-Olette et al., 2009, 2010). However, this phytoremediation can only be applied to remove dimethomorph from wastewater but not from soil and its removal effect is slow and time-consuming. Recently, biodegradation using active microbes offers an alternative to detoxify toxic pollutants from water or soil (Jiang et al., 2016; Zhang et al., 2019). Jia and Zhu (2015) found that Enterobacter sp. QD26-6 could degrade 26.60% of 100 mg/L dimethomorph in Minimal salt medium (MSM) after inoculation for 72 h. Suryawanshi et al. (2018) reported that Bacillus subtilis DR-39 enhanced dimethomorph degradation in grape under the field condition after 15 and 30 d of application (<20% of degradation efficiency). Obviously, the two strains mentioned above could not effectively degrade dimethomorph, which largely limited their practical utilization in the bioremediation of dimethomorph-polluted in situ due to the influence of the multiple environmental factors.

The success of the degradation or removal of pollutants using active microbes is dependent on their survival or adaptability after being released into the pollutant habitat (Liu et al., 2018; Cai et al., 2011), which can be improved by immobilizing microbes with the matrix acting as a nutrient source (e.g. BC) (Liu et al., 2012b; Shi et al., 2018). As an ideal immobilization matrix, BC possesses the large specific surface area, strong adsorption ability and high porosity to guarantee higher cell density and permeability of microbes (Zhang et al., 2019; Shi et al., 2018; Qiao et al., 2010). Moreover, immobilization of microbes with BC makes them more tolerance to toxicity of hazardous pollutants and more insensitiveness to pH, temperature, and salinity changes (Zhang et al., 2019; Qiao et al., 2010; More et al., 2015; Lim et al., 2018; Zhang et al., 2020). Therefore, BC was frequently used as matrices for microbe immobilization, which has been demonstrated to be especially rapid for degrading or removing toxic pollutant in cases of pyridine (Qiao et al., 2010), pendimethalin (More et al., 2015), 4-chloropheno (Lim et al., 2018), and dimethachlon (Zhang et al., 2019, 2020).

This study isolated the novel dimethomorph-degrading strain B. cereus WL08 from soils long term exposed to dimethomorph. Immobilized systems of WL08 were developed with the immobilization matrix incorporated with BC and SA. The biodegradation conditions of dimethomorph by free and immobilize WL08 were optimized on the basis of its degradative efficiencies under variable conditions, and the metabolic pathway of dimethomorph under the optimal conditions was investigated. Furthermore, the reusability and storage stability of free and immobilized WL08 were evaluated. Finally, the removal efficiencies of dimethomorph from water in the continuous reactor and outdoor field soil using immobilized WL08 were demonstrated. Immobilized WL08 can be considered as a tool for the removal of dimethomorph from water and soil. This study provides the first microbe-based strategy for application in bioremediation of dimethomorph-polluted water-soil systems in situ.

Section snippets

Chemicals and medium

Dimethomorph with 99.0 percent purity was purchased from Dr. Ehrenstorfer GmbH, Germany. 80% dimethomorph WDG was purchased from Jiangsu Huifeng Bio-agriculture Co. Ltd., China. BC with particle size of 0.60 mm was purchased from Shanghai Hainuo charcoal Co. Ltd., China. SA and other chemicals and reagents used in the experiments were analytical grade or HPLC grade. MSM (g/L): MgSO4·H2O 0.20 g, KH2PO4 0.8 g, FeSO4·7H2O 0.005 g, K2HPO4 0.2 g, Na2MoO4 0.003 g, CaSO4 0.1 g, (NH4)2SO4 1.0 g.

Isolation and identification of strain WL08

The novel pure strain WL08 of dimethomorph-degrading was isolated from soil long term exposed to dimethomorph using the enrichment technique. The colony of strain WL08 was approximately 2.0–4.0 mm in diameter, slightly glossy, white, irregular edges and soft cells after cultivation for 3 d on MSM plates supplemented with dimethomorph at 30 ℃. The morphological and physio-biochemical characteristics of strain WL08 are shown in Table 1.

A Blast search of GenBank indicates that the sequence (1429

Conclusions

The novel pure strain efficiently capable of degrading dimethomorph was isolated from its polluted soil and identified as B. cereus WL08. Bamboo charcoal and sodium alginate were used as immobilization matrices to develop the immobilized system of WL08, whose biodegradation conditions for dimethomorph were optimized together with free WL08 under variable conditions. Strain WL08 efficiently degraded dimethomorph to simple products less toxic than their parent compound. Immobilization of WL08

Credit Author Statement

Cheng Zhang, Xiaomao Wu and Yongquan Zheng conceived and designed the experiments; Cheng Zhang, Jiaohong Li, Youhua Long and Huaming An performed the experiments; Cheng Zhang, Xinglu Pan, Ming Li and Fengshou Dong analyzed the data; Cheng Zhang, Xiaomao Wu and Yongquan Zheng wrote the paper. All authors have read and agreed to the published version of the manuscript.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. We declare that we do not have any commercial or associative interest that represents a conflict of interest in connection with the work submitted.

Acknowledgments

This work was supported by the Joint Fund of the National Natural Science Foundation of China and the Karst Science Research Center of Guizhou Province (No. U1812401), the National Natural Science Foundation of China [No. 21267007], the Science-Technology Support Program of Guizhou Province [No. (2017)2568, [2018]2351, [2019]2403, [2019]2407, [2019]2272, [2020]1Y134], and the Foundation of Excellent Youth Science-Technology Talent of Guizhou Province [No. (2017)5616].

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