Rapid degradation of dimethomorph in polluted water and soil by Bacillus cereus WL08 immobilized on bamboo charcoal–sodium alginate
Graphical abstract
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].
References (47)
- et al.
Phototransformation pathways of the fungicide dimethomorph ((E, Z) 4-[3-(4-chlorophenyl)-3-(3, 4-dimethoxyphenyl)-1-oxo-2-propenyl] morpholine), relevant to sunlit surface waters
Sci. Total Environ.
(2014) - et al.
Phenol degradation by Bacillus cereus: pathway and kinetic modeling
Bioresour. Technol.
(2010) - et al.
Phenol degradation performance by isolated Bacillus cereus immobilized in alginate
Int. Biodeter. Biodegr.
(2011) - et al.
The biodegradation pathway of triethylamine and its biodegradation by immobilized Arthrobacter protophormiae cells
J. Hazard. Mater.
(2011) - et al.
Enhancement of cypermethrin degradation by a coculture of Bacillus cereus ZH-3 and Streptomyces aureus HP-S-01
Bioresour. Technol. Rep.
(2012) - et al.
Responses of indigenous microorganisms to a fungicidal mixture of mancozeb and dimethomorph added to sandy soils
Int. Biodeter. Biodegr.
(2010) - et al.
Inoculated Clitoria ternatea with Bacillus cereus ERBP for enhancing gaseous ethylbenzene phytoremediation: plant metabolites and expression of ethylbenzene degradation genes
Ecotox. Environ. Safe.
(2018) - et al.
Formation of soluble Cr(III) end-products and nanoparticles during Cr(VI) reduction by Bacillus cereus strain XMCr-6
Biochem. Eng. J.
(2013) - et al.
Phytoremediation of fungicides by aquatic macrophytes: toxicity and removal rate
Ecotox. Environ. Safe.
(2009) - et al.
Influence of initial pesticide concentrations and plant population density on dimethomorph toxicity and removal by two duckweed species
Ecotox. Environ. Safe.
(2010)
An eco-friendly detoxification of chlorpyrifos by Bacillus cereus MCAS02 native isolate from agricultural soil, Namakkal, Tamil Nadu, India
Biocatal. Agric. Biotechnol.
Bioaccumulation characterization of cadmium by growing Bacillus cereus RC-1 and its mechanism
Chemosphere.
A novel integration system of magnetically immobilized cells and a pair of graphite plate-stainless iron mesh electrodes for the bioremediation of coking wastewater
Bioresour. Technol. Rep.
Self-mediated pH changes in culture medium affecting biosorption and biomineralization of Cd 2+ by Bacillus cereus Cd01
J. Hazard. Mater.
Dissipation and residue of dimethomorph in pepper and soil under field conditions
Ecotox. Environ. Safe.
Shielding immobilized biomass cryogel beads with powdered activated carbon for the simultaneous adsorption and biodegradation of 4-chlorophenol
J. Clean. Prod.
Behavior of mixed formulation of metalaxyl and dimethomorph in grape and soil under field conditions
Ecotox. Environ. Safe.
Removal of nitrate using Paracoccus sp. YF1 immobilized on bamboo carbon
J. Hazard. Mater.
Removal of nitrate using Paracoccus sp. YF1 immobilized on bamboo carbon
J. Hazard. Mater.
Characterization of cell-free extracts from fenpropathrin-degrading strain Bacillus cereus ZH-3 and its potential for bioremediation of pyrethroid-contaminated soils
Sci. Total Environ.
Isolation, identification, and crude oil degradation characteristics of a high-temperature, hydrocarbon-degrading strain
Mar. Pollut. Bull.
Enhanced degradation of prometryn and other s-triazine herbicides in pure cultures and wastewater by polyvinyl alcohol-sodium alginate immobilized Leucobacter sp. JW-1
Sci. Total Environ.
Carbon-fibre microelectrodes coupled with square-wave voltammetry for the direct analysis of dimethomorph fungicide in natural waters
Microchem. J.
Cited by (52)
Evaluating pesticide degradation in artificial wetlands with compound-specific isotope analysis: A case study with the fungicide dimethomorph
2023, Science of the Total EnvironmentMetagenomics insights into the performance and mechanism of soil infiltration systems on removing antibiotic resistance genes in rural sewage
2023, Journal of Environmental Management