Article Cite This: J. Agric. Food Chem. 2019, 67, 6683−6690
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Toxicity and Metabolic Fate of the Fungicide Carbendazim in the Typical Freshwater Diatom Navicula Species Tengda Ding,* Wen Li, and Juying Li* Shenzhen Key Laboratory of Environmental Chemistry and Ecological Remediation, College of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, Guangdong 518060, People’s Republic of China
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S Supporting Information *
ABSTRACT: Fungicides are frequently detected in natural water and have gained increasing attention as a result of their potential toxicity to non-target aquatic organisms. Carbendazim (CAR), a commonly used fungicide, was selected to explore its toxicity and biodegradation in a typical freshwater diatom Navicula sp. Results showed that the growth of Navicula sp. was inhibited by CAR, with a 24 h EC50 value of 2.18 mg L−1. Although the algal growth rate was recovered after 72 h of exposure, the chlorophyll a content remained significantly decreased when the concentration of CAR was above 0.5 mg L−1. Moreover, Navicula sp. had a negative effect on the removal of CAR, and the acute toxicity by CAR was likely due to its rapid accumulation in algal cells. Mass spectrometric data revealed the transformation products of CAR from hydroxylation, methylation, decarboxylation, demethylation, and deamination in algal cultures. These results provide a better understanding of the environmental risks of CAR in water and point to the need for additional studies on the potential adverse biological effects of its intermediates. KEYWORDS: carbendazim, toxicity, biodegradation, metabolism, Navicula sp.
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INTRODUCTION The environmental effects of a common fungicide carbendazim (methyl-2-benzimidazole carbamate, CAR) are well-documented because it is widely used in the agricultural field.1−3 As a result of its high toxicity to non-target organisms, CAR has been banned for use in some developed countries (e.g., Australia and the U.S.A.); however, it is still produced and used in developing countries, such as China, Brazil, and India.3 For instance, the sales of CAR accounted for approximately 1% of total pesticide use in Brazil in 2015.4 Additionally, CAR is one of the transformation products of benomyl and thiophanate methyl pesticides under natural conditions,5 leading to the increased environmental occurrence of CAR. The frequent application of CAR results in its accumulation in soil and natural water through surface runoff or leachate. For example, CAR was frequently detected in the receiving water around the agricultural fields with a concentration of 0.5 μg L−1 with the application of 14.7 kg ha−1 pesticides, suggesting a high risk for the ecosystem.6 Chatupote and Panapitukkul reported that CAR was detected in the Rattaphum catchment of Thailand with the concentration of 4.5 μg L−1.7 CAR was also detected in surface water, which were located in the agricultural area with the maximum concentration of 156 μg L−1.4,8 Additionally, CAR is highly persistent in natural water with half-lives of 6−25 weeks,9 suggesting that CAR tended to accumulate in freshwater with the potential for long-term effects. Liu et al. reported high ecological risks posed by CAR in the Yangtze River.10 For example, CAR posed a toxic effect on crustacean,11 invertebrates,9 and fish.12 In aquatic food chains, algae play an important role as important primary producers for other aquatic organisms and are usually used to evaluate the environmental risks of pollutants in the aquatic environment. CAR was reported to pose a toxic effect to © 2019 American Chemical Society
aquatic organisms. For example, the growth rates of aquatic submerged plants Elodea nuttalli and Myriophyllum spicatum were significantly decreased by CAR, with the median effective concentrations (EC50) of 330 and 10 000 μg L−1, respectively [Pesticide Action Network (PAN) Pesticide Database and Ecotoxicology Database (ECOTOX)].13 Similarly, Ma et al. reported that CAR could inhibit the growth of Chlorella pyrenoidosa and Scenedesmus obliqnus, with the 96 h EC50 of 34.7 and 19.1 mg L−1, respectively.14 In addition, CAR was recalcitrant to the conventional activated sludge processes with a removal rate of 0.25 mg L−1 after 72 h of exposure, implying that oxidative damage on the algal chloroplast may occur. The rapid degradation of CAR occurred in the D1 medium. The degradation was significantly inhibited by the addition of Navicula sp. Five biodegradation metabolites of CAR were identified in algal cells. The findings in this study suggested a potential toxicity of CAR in the natural water, and the bioavailability of its metabolites to nontarget organisms merits further investigation.
Article
ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.8b06179. Variations of the algal growth rate under CAR exposure at different incubation times (Figure S1), degradation percentage of CAR in (a) pure medium and (b) Navicula sp. culutres during the incubation time (Figure S2), chromatograms of CAR metabolites in Navicula sp. cultures with an initial CAR concentration of 500 μg L−1 (Figure S3), MS spectra in the identification process of TP 143 in Navicula sp. (Figure S4), MS spectra in the identification process of TP 157 in Navicula sp. (Figure S5), MS spectra in the identification process of TP 193 in Navicula sp. (Figure S6), MS spectra in the identification process of TP 135 in Navicula sp. (Figure S7), MS spectra in the identification process of TP 103 in Navicula sp. (Figure S8), MS spectra in the identification process of TP 130 in the D1 medium (Figure S9), and peak area kinetics of CAR metabolites in the (a) Navicula sp. cells and (b) D1 medium during 144 h of incubation (Figure S10) (PDF)
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AUTHOR INFORMATION
Corresponding Authors
*E-mail:
[email protected]. *E-mail:
[email protected]. ORCID
Tengda Ding: 0000-0002-0551-9712 Juying Li: 0000-0003-1294-241X Funding
This research was financially supported by the National Natural Science Foundation of China (Grants 21607106 and 21777104), the Natural Science Foundation of Guangdong Province (2017A030313226), the Shenzhen Science and Technology Project (Grant JCYJ20170818142823471), the Natural Science Foundation of Shenzhen University (SZU) (Grant 2019027), and the Environmental Protection Industry Development Special Fund of Shenzhen. The authors also very much appreciate the polishing of the manuscript by Dr. Chunlong Zhang at University of HoustonClear Lake, Houston, TX, U.S.A. Notes
The authors declare no competing financial interest.
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ABBREVIATIONS USED CAR, carbendazim; UPLC−MS/MS, ultra performance liquid chromatography−tandem mass spectrometry; HPLC, highperformance liquid chromatography; BCF, bioconcentration factor
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REFERENCES
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DOI: 10.1021/acs.jafc.8b06179 J. Agric. Food Chem. 2019, 67, 6683−6690
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