Abstract
The microbial fuel cell (MFC) provides an inexhaustible electron acceptor to generate current and enhance the degradation of organic compounds. In MFCs with metolachlor as the sole carbon source, the degradation efficiency accelerated by 98%, with 61–76% of enhancement for the degradates, ethane sulfonic acid and oxanilic acid, respectively. According to quantifying primary metabolites of deschloro and metolachlor-2-hydroxyas, dechlorination and alcoholization were deemed as antecedent steps of metolachlor bioelectrochemical degradation. The energy recovery was infeasible by sole addition of metolachlor (at 13 ± 4 °C from equivalent weight of 0.224 mg). In MFCs with metolachlor and sodium acetate as the concomitant carbon sources, the electricity generation recovered to a level comparable to the controls, instead of increasing the removal efficiency of metolachlor. These results suggest that a low-efficiently direct electron transfer occurred between electricigens and metolachlor degraders. The Illumina sequencing showed that species of Paracoccus and Aquamicrobium played a potential degradation effect, while Comamonas sp. replaced Geobacter sp. as the predominant electricigen after addition of metolachlor. This study demonstrates that MFCs could be used as a promising alternative for treatment of chloroacetanilide herbicide contaminated wastewaters by means of a rapidly established active bacterial community.
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References
Cao, X., Song, H., Yu, C., & Li, X. (2015). Simultaneous degradation of toxic refractory organic pesticide and bioelectricity generation using a soil microbial fuel cell. Bioresource Technology, 189, 87–93.
Defeng, X., Shaoan, C., Regan, J. M., & Logan, B. E. (2010). Change in microbial communities in acetate- and glucose-fed microbial fuel cells in the presence of light. Biosensors & Bioelectronics, 25, 105–111.
Dubbels, B. L., Sayavedra-Soto, L. A., Bottomley, P. J., & Arp, D. J. (2009). Thauera butanivorans sp. nov., a C2-C9 alkane-oxidizing bacterium previously referred to as ‘Pseudomonas butanovora’. International Journal of Systematic and Evolutionary Microbiology, 59(7), 1576–1578.
Dwivedi, S., Singh, B. R., Al-Khedhairy, A. A., Alarifi, S., & Musarrat, J. (2010). Isolation and characterization of butachlor-catabolizing bacterial strain Stenotrophomonas acidaminiphila JS-1 from soil and assessment of its biodegradation potential. Letters in Applied Microbiology, 51, 54–60.
Fenner, K., Canonica, S., Wackett, L. P., & Elsner, M. (2013). Evaluating pesticide degradation in the environment: Blind spots and emerging opportunities. Science, 341(6147), 752–758.
Foley, M. E., Sigler, V., & Gruden, C. L. (2008). A multiphasic characterization of the impact of the herbicide acetochlor on freshwater bacterial communities. The ISME Journal, 2(1), 56–66.
Friedman, C. L., And, A. T. L., & Hay, A. (2006). Degradation of chloroacetanilide herbicides by anodic Fenton treatment. Journal of Agricultural and Food Chemistry, 54(7), 2640–2651.
Hartnett, S., Musah, S., & Dhanwada, K. R. (2013). Cellular effects of metolachlor exposure on human liver (HepG2) cells. Chemosphere, 90(3), 1258–1266.
Hladik, M. L., Bouwer, E. J., & Roberts, A. L. (2008). Neutral chloroacetamide herbicide degradates and related compounds in Midwestern United States drinking water sources. The Science of the Total Environment, 390(1), 155–165.
Iwata, S., Ostermeier, C., Ludwig, B., & Michel, H. (1995). Structure at 2.8 A resolution of cytochrome c oxidase from Paracoccus denitrificans. Nature, 376(6542), 660–669.
Kalkhoff, S. J., Kolpin, D. W., Thurman, E. M., Ferrer, I., & Barcelo, D. (1998). Degradation of chloroacetanilide herbicides: The prevalence of sulfonic and oxanilic acid metabolites in Iowa groundwaters and surface waters. Environmental Science & Technology, 32(11), 1738–1740.
Kumru, M., Eren, H., Catal, T., Bermek, H., & Akarsubaşi, A. T. (2012). Study of azo dye decolorization and determination of cathode microorganism profile in air-cathode microbial fuel cells. Environmental Technology, 33(18), 2167–2175.
Li, X., Wang, X., Zhang, Y., Ding, N., & Zhou, Q. (2014). Opening size optimization of metal matrix in rolling-pressed activated carbon air–cathode for microbial fuel cells. Applied Energy, 123, 13–18.
Li, X., Wang, X., Wan, L., Zhang, Y., Li, N., Li, D., & Zhou, Q. (2016). Enhanced biodegradation of aged petroleum hydrocarbons in soils by glucose addition in microbial fuel cells. Journal of Chemical Technology and Biotechnology, 91(1), 267–275.
Li, Y., Li, X., Sun, Y., Zhao, X., & Li, Y. (2018). Cathodic microbial community adaptation to the removal of chlorinated herbicide in soil microbial fuel cells. Environemental Science and Pollution Research, 25(17), 16900–16912.
Liu, H., Huang, R., Xie, F., Zhang, S., & Shi, J. (2012). Enantioselective phytotoxicity of metolachlor against maize and rice roots. Journal of Hazardous Materials, s 217–218, 330–337.
Logan, B. E., & Rabaey, K. (2012). Conversion of wastes into bioelectricity and chemicals by using microbial electrochemical technologies. Science, 337(6095), 686–690.
Lovley, D. R. (2008). The microbe electric: conversion of organic matter to electricity. Current Opinion in Biotechnology, 19(6), 564–571.
Lovley, D. R., & Phillips, E. J. (1988). Novel mode of microbial energy metabolism: Organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Applied and Environmental Microbiology, 54, 1472–1480.
Mao, Y., Xia, Y., & Zhang, T. (2013). Characterization of Thauera-dominated hydrogen-oxidizing autotrophic denitrifying microbial communities by using high-throughput sequencing. Bioresource Technology, 128, 703–710.
Phillips, P. J., Wall, G. R., Thurman, E. M., & Eckhardt, D. A. (1999). Metolachlor and its metabolites in tile drain and stream runoff in the Canajoharie Creek watershed. Environmental Science & Technology, 33(20), 3531–3537.
Postle, J. K., Rheineck, B. D., Allen, P. E., Baldock, J. O., Cook, C. J., Zogbaum, R., & Vandenbrook, J. P. (2004). Chloroacetanilide herbicide metabolites in Wisconsin groundwater: 2001 survey results. Environmental Science & Technology, 38(20), 5339–5343.
Rabaey, K., & Willy, V. (2005). Microbial fuel cells: Novel biotechnology for energy generation. Trends in Microbiology, 23, 291–298.
Rebich, R. A., Coupe, R. H., & Thurman, E. M. (2004). Herbicide concentrations in the Mississippi River Basin—The importance of chloroacetanilide herbicide degradates. The Science of the Total Environment, 321(1-3), 189–199.
Seybold, C. A., Mersie, W., & Mcnamee, C. (2001). Anaerobic degradation of atrazine and metolachlor and metabolite formation in wetland soil and water microcosms. Journal of Environmental Quality, 30(4), 1271.
Trigo, C., Spokas, K., Hall, K., Cox, L., & Koskinen, W. C. (2016). Metolachlor sorption and degradation in soil amended with fresh and aged biochars. Journal of Agricultural and Food Chemistry, 64(16), 3141–3149.
Urakami, T., Araki, H., Oyanagi, H., Suzuki, K., & Komagata, K. (1990). Paracoccus aminophilus sp. nov. and Paracoccus aminovorans sp. nov., which utilize N,N-dimethylformamide. International Journal of Systematic Bacteriology, 40(3), 287–291.
Walling, C., Eltaliawi, G. M., & Johnson, R. A. (1974). Fenton's reagent. IV. Structure and reactivity relations in the reactions of hydroxyl radicals and the redox reactions of radicals. Journal of the American Chemical Society, 96, 10015–10017.
Wan, Y., Zhou, L., Wang, S., Liao, C., Li, N., Liu, W., & Wang, X. (2018). Syntrophic growth of Geobacter sulfurreducens accelerates anaerobic denitrification. Frontiers in Microbiology, 9, 1572.
Wang, X., Cheng, S., Feng, Y., Merrill, M. D., Saito, T., & Logan, B. E. (2009). Use of carbon mesh anodes and the effect of different pretreatment methods on power production in microbial fuel cells. Environmental Science & Technology, 43(17), 6870–6874.
Wang, H., Luo, H., Fallgren, P. H., Jin, S., & Ren, Z. J. (2015). Bioelectrochemical system platform for sustainable environmental remediation and energy generation. Biotechnology Advances, 33(3-4), 317–334.
Woodward, E. E., Hladik, M. L., & Kolpin, D. W. (2018). Occurrence of dichloroacetamide herbicide safeners and co-applied herbicides in midwestern U.S. streams. Environmental Science & Technology Letters, 5(1), 3–8.
World Health Organization. (1993). Guidelines for drinking-water quality (Vol. 1, 2nd ed.). Geneva: World Health Organization.
Wu, J., Jiang, C., Wang, B., Ma, Y., Liu, Z., & Liu, S. (2006). Novel partial reductive pathway for 4-chloronitrobenzene and nitrobenzene degradation in Comamonas sp. strain CNB-1. Applied and Environmental Microbiology, 72(3), 1759–1765.
Wu, Y., Zaiden, N., & Cao, B. (2018). The core-and pan-genomic analyses of the genus Comamonas: from environmental adaptation to potential virulence. Frontiers in Microbiology, 9, 3096.
Xing, D., Cheng, S., Logan, B. E., & Regan, J. M. (2010). Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Applied Microbiology and Biotechnology, 85(5), 1575–1587.
Xu, G. M., Zheng, Y. Y., Wang, S. H., Zhang, J. S., & Yan, Y. C. (2008). Biodegradation of chlorpyrifos and 3,5,6-trichloro-2-pyridinol by a newly isolated Paracoccus sp. strain TRP. International Biodeterioration & Biodegradation, 62(1), 51–56.
Yu, Y., Wu, Y., Cao, B., Gao, Y. G., & Yan, X. (2015). Adjustable bidirectional extracellular electron transfer between Comamonas testosteroni biofilms and electrode via distinct electron mediators. Electrochemistry Communications, 59, 43–47.
Zhang, J., Zheng, J. W., Liang, B., Wang, C. H., Cai, S., Ni, Y. Y., He, J., & Li, S. P. (2011). Biodegradation of chloroacetamide herbicides by Paracoccus sp. FLY-8 in vitro. Journal of Agricultural and Food Chemistry, 59(9), 4614–4621.
Zhang, Y., Wang, X., Li, X., Gao, N., Wan, L., Feng, C., & Zhou, Q. (2014). A novel and high performance activated carbon air-cathode with decreased volume density and catalyst layer invasion for microbial fuel cells. RSC Advances, 4(80), 42577–42580.
Funding
This study was financially supported by the National Key R&D Program of China (No. 2017YFD0800704), the National Natural Science Foundation of China (No. 41601536 and 31500425), the Natural Science Foundation of Tianjin city of China (No. 16JCQNJC08800), the Opening Foundation of Ministry of Education of China Key Laboratory of Pollution Processes and Environmental Criteria (2017-05), and the Central Public-interest Scientific Institution Basal Research Fund.
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Highlight
• The removal efficiency of metolachlor enhanced by 98% in MFCs.
• Contents of the degradates MESA and MOA were 61–76% lower than controls.
• The dechlorination was the antecedent step by quantifying primary metabolites.
• Species of Paracoccus and Aquamicrobium played a potential degradation effect.
• Comamonas instead of Geobacter was responsible for the electricity generation.
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Li, X., Zhang, X., Zhao, X. et al. Efficient Removal of Metolachlor and Bacterial Community of Biofilm in Bioelectrochemical Reactors. Appl Biochem Biotechnol 189, 384–395 (2019). https://doi.org/10.1007/s12010-019-03014-0
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DOI: https://doi.org/10.1007/s12010-019-03014-0