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Cathodic microbial community adaptation to the removal of chlorinated herbicide in soil microbial fuel cells

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Abstract

The microbial fuel cell (MFC) that uses a solid electrode as the inexhaustible electron acceptor is an innovative remediation technology that simultaneously generates bioelectricity. Chlorinated pollutants are better metabolized by reductive dechlorination in proximity to the cathode. Here, the removal efficiency of the herbicide metolachlor (ML) increased by 262 and 176% in soil MFCs that were spiked with 10 (C10) and 20 mg/kg (C20) of ML, respectively, relative to the non-electrode controls. The bioelectricity output of the C10 and C20 increased by over two- and eightfold, respectively, compared to that of the non-ML control, with maximum current densities of 49.6 ± 2.5 (C10) and 78.9 ± 0.6 mA/m2 (C20). Based on correlations between ML concentrations and species abundances in the MFCs, it was inferred that Azohydromonas sp., Sphingomonas sp., and Pontibacter sp. play a major role in ML removal around the cathode, with peak removal efficiencies of 56 ± 1% (C10) and 58 ± 1% (C20). Moreover, Clostridium sp., Geobacter sp., Bacillus sp., Romboutsia sp., and Terrisporobacter sp. may be electricigens or closely related microbes due to the significant positive correlation between the bioelectricity generation levels and their abundances around the anode. This study suggests that a directional adaptation of the microbial community has taken place to increase both the removal of chlorinated herbicides around the cathode and the generation of bioelectricity around the anode in bioelectrochemical remediation systems.

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References

  • Accinelli C, Dinelli G, Vicari A, Catizone P (2001) Atrazine and metolachlor degradation in subsoils. Biol Fertil Soils 33:495–500

    Article  CAS  Google Scholar 

  • Adamczyk B, Kitunen V, Smolander A (2009) Polyphenol oxidase, tannase and proteolytic activity in relation to tannin concentration in the soil organic horizon under silver birch and Norway spruce. Soil Biol Biochem 41:2085–2093

    Article  CAS  Google Scholar 

  • Arora PK, Sasikala C, Ramana Ch V (2012) Degradation of chlorinated nitroaromatic compounds. Appl Microbiol Biotechnol 93:2265–2277

    Article  CAS  Google Scholar 

  • Bardot C, Besse-Hoggan P, Carles L, Le Gall M, Clary G, Chafey P, Federici C, Broussard C, Batisson I (2015) How the edaphic Bacillus megaterium strain Mes11 adapts its metabolism to the herbicide mesotrione pressure. Environ Pollut 199:198–208

    Article  CAS  Google Scholar 

  • Borah D, More S, Yadav RNS (2013) Construction of double chambered microbial fuel cell (MFC) using household materials and Bacillus metaterium isolate from tea garden soil. J Microbiol Biotechnol Food Sci 3:84–86

    CAS  Google Scholar 

  • 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. Bioresour Technol 189:87–93

    Article  CAS  Google Scholar 

  • Cao X, Yu C, Wang H, Zhou F, Li X (2017) Simultaneous degradation of refractory organic pesticide and bioelectricity generation in a soil microbial fuel cell with different conditions. Environ Technol 38:1043–1050

    Article  CAS  Google Scholar 

  • Colman S, Linderman R, Hodgson E, Rose RL (2000) Comparative metabolism of chloroacetamide herbicides and selected metabolites in human and rat liver microsomes. Environ Health Perspect 108:1151–1157

    Google Scholar 

  • Feng X, Zhu M, He Y (2017) Effects and mechanisms of soil redox processes on reductive dechlorination of chlorinated organic pollutants. Asian J Ecotox 12:151–161

    Google Scholar 

  • Gundi VA, Viswanath B, Chandra MS, Kumar VN, Reddy BR (2007) Activities of cellulase and amylase in soils as influenced by insecticide interactions. Ecotox Environ Safe 68:278–285

    Article  CAS  Google Scholar 

  • Hartnett S, Musah S, Dhanwada KR (2013) Cellular effects of metolachlor exposure on human liver (HepG2) cells. Chemosphere 90:1258–1266

    Article  CAS  Google Scholar 

  • Huang D, Zhou S, Chen Q, Zhao B, Yuan Y, Zhuang L (2011) Enhanced anaerobic degradation of organic pollutants in a soil microbial fuel cell. Chem Eng J 172:647–653

    Article  CAS  Google Scholar 

  • Konstantinou IK, Hela DG, Albanis TA (2006) The status of pesticide pollution in surface waters (rivers and lakes) of Greece. Part I. Review on occurrence and levels. Environ Pollut 141:555–570

    Article  CAS  Google Scholar 

  • Li X, Wang X, Zhang Y, Cheng L, Liu J, Li F, Gao B, Zhou Q (2014a) Extended petroleum hydrocarbon bioremediation in saline soil using Pt-free multianodes microbial fuel cells. RSC Adv 4:59803–59808

    Article  CAS  Google Scholar 

  • Li X, Wang X, Zhang Y, Ding N, Zhou Q (2014b) Opening size optimization of metal matrix in rolling-pressed activated carbon air-cathode for microbial fuel cells. Appl Energy 123:13–18

    Article  CAS  Google Scholar 

  • Li X, Wang X, Ren ZJ, Zhang Y, Li N, Zhou Q (2015) Sand amendment enhances bioelectrochemical remediation of petroleum hydrocarbon contaminated soil. Chemosphere 141:62–70

    Article  CAS  Google Scholar 

  • Li X, Wang X, Wan L, Zhang Y, Li N, Li D, Zhou Q (2016a) Enhanced biodegradation of aged petroleum hydrocarbons in soils by glucose addition in microbial fuel cells. J Chem Technol Biotechnol 91:267–275

    Article  CAS  Google Scholar 

  • Li X, Wang X, Zhang Y, Zhao Q, Yu B, Li Y, Zhou Q (2016b) Salinity and conductivity amendment of soil enhanced the bioelectrochemical degradation of petroleum hydrocarbons. Sci Rep 6:32861

    Article  CAS  Google Scholar 

  • Li X, Wang X, Weng L, Zhou Q, Li Y (2017) Microbial fuel cells for organic-contaminated soil remedial applications: a review. Energy Technol 5:1156–1164

    Article  CAS  Google Scholar 

  • Liu G (1996) Soil physical and chemical analysis and description of soil profiles. Standard Press, Beijing

    Google Scholar 

  • Liu H, Ye W, Zhan X, Liu W (2006) A comparative study of rac- and S-metolachlor toxicity to Daphnia magna. Ecotox Environ Safe 63:451–455

    Article  CAS  Google Scholar 

  • Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381

    Article  CAS  Google Scholar 

  • Logan BE, Regan JM (2006) Electricity-producing bacterial communities in microbial fuel cells. Trends Microbiol 14:512–518

    Article  CAS  Google Scholar 

  • Logan BE, Hamelers B, Rozendal R, Schroder U, Keller J, Verstraete W, Rabaey K (2006) Microbial fuel cells methodology and technology. Environ Sci Technol 40:5181–5192

    Article  CAS  Google Scholar 

  • Lovley DR (2006) Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4:497–508

    Article  CAS  Google Scholar 

  • Lovley DR (2008) The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 19:564–571

    Article  CAS  Google Scholar 

  • Lovley DR (2011) Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ Microbiol Rep 3:27–35

    Article  CAS  Google Scholar 

  • Lu L, Huggins T, Jin S, Zuo Y, Ren ZJ (2014a) Microbial metabolism and community structure in response to bioelectrochemically enhanced remediation of petroleum hydrocarbon-contaminated soil. Environ Sci Technol 48:4021–4029

    Article  CAS  Google Scholar 

  • Lu L, Yazdi H, Jin S, Zuo Y, Fallgren PH, Ren ZJ (2014b) Enhanced bioremediation of hydrocarbon-contaminated soil using pilot-scale bioelectrochemical systems. J Hazard Mater 274:8–15

    Article  CAS  Google Scholar 

  • Morris JM, Song J (2012) Enhanced biodegradation of hydrocarbon-contaminated sediments using microbial fuel cells. J Hazard Mater 213-214:474–477

    Article  CAS  Google Scholar 

  • Mulla SI, Hu A, Wang Y, Sun Q, Huang S, Wang H, Yu C (2016) Degradation of triclocarban by a triclosan-degrading Sphingomonas sp. strain YL-JM2C. Chemosphere 144:292–296

    Article  CAS  Google Scholar 

  • Ng EL, Patti AF, Rose MT, Schefe CR, Wilkinson K, Cavagnaro TR (2014) Functional stoichiometry of soil microbial communities after amendment with stabilised organic matter. Soil Biol Biochem 76:170–178

    Article  CAS  Google Scholar 

  • Quejigo JR, Domínguez-Garay A, Dörfler U, Schroll R, Esteve-Núñez A (2018) Anodic shifting of the microbial community profile to enhance oxidative metabolism in soil. Soil Biol Biochem 116:131–138

    Article  CAS  Google Scholar 

  • Quilchano C, Marañón T (2002) Dehydrogenase activity in Mediterranean forest soils. Biol Fert Soils 35:102–107

    Article  CAS  Google Scholar 

  • Rabaey K, Willy V (2005) Microbial fuel cells: novel biotechnology for energy generation. Trends Microbiol 23:291–298

    CAS  Google Scholar 

  • Santoro C, Guilizzoni M, Correa Baena JP, Pasaogullari U, Casalegno A, Li B, Babanova S, Artyushkova K, Atanassov P (2014) The effects of carbon electrode surface properties on bacteria attachment and start up time of microbial fuel cells. Carbon 67:128–139

    Article  CAS  Google Scholar 

  • Singh AK, Garg N, Lata P, Kumar R, Negi V, Vikram S, Lal R (2014) Pontibacter indicus sp. nov., isolated from hexachlorocyclohexane-contaminated soil. Int J Syst Evol Microbiol 64:254–259

    Article  CAS  Google Scholar 

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • Strycharz SM, Gannon SM, Boles AR, Franks AE, Nevin KP, Lovley DR (2010) Reductive dechlorination of 2-chlorophenol by Anaeromyxobacter dehalogenans with an electrode serving as the electron donor. Environ Microbiol Rep 2:289–294

    Article  CAS  Google Scholar 

  • Trigo C, Spokas K, Hall K, Cox L, Koskinen WC (2016) Metolachlor sorption and degradation in soil amended with fresh and aged biochars. J Agric Food Chem 64:3141–3149

    Article  CAS  Google Scholar 

  • Vryzas Z, Alexoudis C, Vassiliou G, Galanis K, Papadopoulou-Mourkidou E (2011) Determination and aquatic risk assessment of pesticide residues in riparian drainage canals in northeastern Greece. Ecotox Environ Safe 74:174–181

    Article  CAS  Google Scholar 

  • Wang X, Cai Z, Zhou Q, Zhang Z, Chen C (2012) Bioelectrochemical stimulation of petroleum 516 hydrocarbon degradation in saline soil using U-tube microbial fuel cells. Biotechnol Bioeng 517 109:426–433

    Article  CAS  Google Scholar 

  • Wang X, Feng C, Ding N, Zhang Q, Li N, Li X, Zhang Y, Zhou Q (2014) Accelerated OH− transport in activated carbon air-cathode by modification of quaternary ammonium for microbial fuel cells. Environ Sci Technol 48:4191–4198

    Article  CAS  Google Scholar 

  • Wang Y, Chen Z, Liu P, Sun G, Ding L, Zhu Y (2016) Arsenic modulates the composition of anode-respiring bacterial community during dry-wet cycles in paddy soils. J Soils Sediments 16:1745–1753

    Article  CAS  Google Scholar 

  • Wang H, Yi S, Cao X, Fang Z, Li X (2017) Reductive dechlorination of hexachlorobenzene subjected to several conditions in a bioelectrochemical system. Ecotox Environ Safe 139:172–178

    Article  CAS  Google Scholar 

  • Wei M, Harnisch F, Vogt C, Ahlheim J, Neu TR, Richnow HH (2015) Harvesting electricity from benzene and ammonium-contaminated groundwater using a microbial fuel cell with an aerated cathode. RSC Adv 5:5321–5330

    Article  CAS  Google Scholar 

  • Wolińska A, Stępniewska Z (2012) Dehydrogenase activity in the soil environment. In: Canuto RA (ed), Dehydrogenases, InTech. https://doi.org/10.5772/48294

  • Wu X, Li M, Long Y, Liu R, Yu Y, Fang H, Li S (2011) Effects of adsorption on degradation and bioavailability of metolachlor in soil. J Soil Sci Plant Nut 11:83–97

    Google Scholar 

  • Xing D, Cheng S, Logan BE, Regan JM (2010) Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Appl Microbiol Biotechnol 85:1575–1587

    Article  CAS  Google Scholar 

  • 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 Adv 4:42577–42580

    Article  CAS  Google Scholar 

  • Zhao Q, Yue S, Bilal M, Hu H, Wang W, Zhang X (2017) Comparative genomic analysis of 26 Sphingomonas and Sphingobium strains: dissemination of bioremediation capabilities, biodegradation potential and horizontal gene transfer. Sci Total Environ 609:1238–1247

    Article  CAS  Google Scholar 

Download references

Funding

This study was financially supported by the Special Fund for Agro-Scientific Research in the Public Interest of China (No. 201503107-7), the Natural Science Foundation of Tianjin (No. 16JCQNJC08800), the National Natural Science Foundation of China (No. 41601536), the National Key R&D Program of China (No. 2017YFD0800704), the Opening Foundation of Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria (2017-05), and the Central Public-interest Scientific Institution Basal Research Fund.

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Authors and Affiliations

  1. College of Land and Environment, Shenyang Agricultural University, Shenyang, 110866, People’s Republic of China

    Yue Li

  2. Agro-Environmental Protection Institute, Ministry of Agriculture, MOA Key Laboratory of Original Agro-Environmental Pollution Prevention and Control, Tianjin, 300191, People’s Republic of China

    Yue Li, Xiaojing Li, Yang Sun, Xiaodong Zhao & Yongtao Li

  3. College of Natural Resources and Environment, South China Agricultural University, Guangzhou, 510642, People’s Republic of China

    Yongtao Li

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  1. Yue Li
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Correspondence to Xiaojing Li.

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Li, Y., Li, X., Sun, Y. et al. Cathodic microbial community adaptation to the removal of chlorinated herbicide in soil microbial fuel cells. Environ Sci Pollut Res 25, 16900–16912 (2018). https://doi.org/10.1007/s11356-018-1871-z

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  • DOI: https://doi.org/10.1007/s11356-018-1871-z

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