Arsenic alleviation in rice by using paddy soil microbial fuel cells

  • Williamson Gustave
  • Zhao-Feng Yuan
  • Yu-Xiang Ren
  • Raju Sekar
  • Jun Zhang
  • Zheng ChenEmail author
Regular Article


Background and aims

Rice (Oryza sativa L.) consumption is a major route of dietary exposure to arsenic (As) in humans. One main reason for the high accumulation of As in rice grain is the high bioavailability of As in porewater of flooded paddy soil. Recently, it has been shown that the application of soil microbial fuel cell (sMFC) can significantly reduce soil porewater As concentration, however, the effect of sMFC on As accumulation in rice is unknown. Hence, this study was aimed at reducing the As uptake in rice grown in As contaminated soil by sMFCs.


A pot experiment was performed to investigate As distribution in rice tissues and the functional microbial communities in soil when the sMFC was installed. The As in the soil porewater and rice plant parts were analyzed. 16S rRNA sequencing and Quantitative PCR were used to examine the microbial community and to quantify the relative abundance of As resistance genes in the rhizosphere, respectively.


The results suggest that the sMFC can simultaneously work as an electricity generator and As mitigator. The total As concentrations in the stems, leaves, husks, and rice grains were significantly decreased by 53.4%, 44.7%, 62.6%, and 67.9%, respectively in the plants with sMFC compared to the control. This decrease in As accumulation in the sMFC treatment may be explained by the decrease in the soil porewater dissolve organic matter content and abundance of As reducing gene (arsC). Moreover, known As reducing classes such as Clostridia, Bacilli and Thermoleophilia were significantly enhanced in the control treatment.


Integrating the sMFC in rice paddy soil offers a promising way to mitigate As accumulation in rice tissue and reduce dietary As exposure, while simultaneously producing electricity.


Rice Soil microbial fuel cell Arsenic Dissolve organic matter Iron 



This work was supported by the National Science Foundation of China (41571305) and Jiangsu Science and Technology Program (BK20161251). The authors acknowledge the kind help of Xiao Zhou and Yi-Li Cheng for their technical support in the sample analysis. The authors are grateful to Elmer Villanueva, Xu Rong and Sun Jing for their help in the statistical, figure drawing and bacterial data analysis, respectively. We also thank Markus Klingelfuss and Jacquelin St. Jean for proof reading the manuscript.

Supplementary material

11104_2019_4098_MOESM1_ESM.docx (102 kb)
ESM 1 (DOCX 101 kb)


  1. Boonyaves K, Wu T-Y, Gruissem W, Bhullar NK (2017) Enhanced grain iron levels in rice expressing an iron-regulated metal transporter, nicotianamine synthase, and ferritin gene cassette. Front Plant Sci 8:130CrossRefGoogle Scholar
  2. Burton ED, Johnston SG, Bush RT (2011) Microbial sulfidogenesis in ferrihydrite-rich environments: effects on iron mineralogy and arsenic mobility. Geochim Cosmochim Acta 75:3072–3087CrossRefGoogle Scholar
  3. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336CrossRefGoogle Scholar
  4. Chen Z, Zhu YG, Liu WJ, Meharg AA (2005) Direct evidence showing the effect of root surface iron plaque on arsenite and arsenate uptake into rice (Oryza sativa) roots. New Phytol 165:91–97CrossRefGoogle Scholar
  5. Chen Z, Huang YC, Liang J-h, Zhao F, Zhu YG (2012) A novel sediment microbial fuel cell with a biocathode in the rice rhizosphere. Bioresour Technol 108:55–59CrossRefGoogle Scholar
  6. Chen Z, Zhu BK, Jia WF, Liang JH, Sun GX (2015) Can electrokinetic removal of metals from contaminated paddy soils be powered by microbial fuel cells? Environ Technol Innov 3:63–67CrossRefGoogle Scholar
  7. Chen C, Huang K, Xie WY, Chen SH, Tang Z, Zhao FJ (2017) Microbial processes mediating the evolution of methylarsine gases from dimethylarsenate in paddy soils. Environmental Science & Technology 51(22):13190–13198Google Scholar
  8. Das S, Liu C-C, Jean J-S, Lee C-C, Yang H-J (2016) Effects of microbially induced transformations and shift in bacterial community on arsenic mobility in arsenic-rich deep aquifer sediments. J Hazard Mater 310:11–19CrossRefGoogle Scholar
  9. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefGoogle Scholar
  10. Gustave W, Yuan Z-F, Sekar R, Chang H-C, Zhang J, Wells M, Ren Y-X, Chen Z (2018) Arsenic mitigation in paddy soils by using microbial fuel cells. Environ Pollut 238:647–655CrossRefGoogle Scholar
  11. Gustave W, Yuan Z-F, Sekar R, Ren Y-X, Chang H-C, Liu J-Y, Chen Z (2019) The change in biotic and abiotic soil components influenced by paddy soil microbial fuel cells loaded. J Soils Sediments 19(1):106–115Google Scholar
  12. Habibul N, Hu Y, Sheng GP (2016a) Microbial fuel cell driving electrokinetic remediation of toxic metal contaminated soils. J Hazard Mater 318:9–14CrossRefGoogle Scholar
  13. Habibul N, Hu Y, Wang YK, Chen W, Yu HQ, Sheng GP (2016b) Bioelectrochemical chromium (VI) removal in plant-microbial fuel cells. Environ Sci Technol 50(7):3882–3889Google Scholar
  14. Hari AR, Venkidusamy K, Katuri KP, Bagchi S, Saikaly PE (2017) Temporal microbial community dynamics in microbial electrolysis cells–influence of acetate and propionate concentration. Front Microbiol 8:1371CrossRefGoogle Scholar
  15. Hashimoto Y, Kanke Y (2018) Redox changes in speciation and solubility of arsenic in paddy soils as affected by sulfur concentrations. Environ Pollut 238:617–623CrossRefGoogle Scholar
  16. Hu ZY, Zhu YG, Li M, Zhang LG, Cao ZH, Smith FA (2007) Sulfur (S)-induced enhancement of iron plaque formation in the rhizosphere reduces arsenic accumulation in rice (Oryza sativa L.) seedlings. Environ Pollut 147:387–393CrossRefGoogle Scholar
  17. Inskeep WP, Macur RE, Hamamura N, Warelow TP, Ward SA, Santini JM (2007) Detection, diversity and expression of aerobic bacterial arsenite oxidase genes. Environ Microbiol 9:934–943CrossRefGoogle Scholar
  18. Jia Y, Sun GX, Huang H, Zhu YG (2013) Biogas slurry application elevated arsenic accumulation in rice plant through increased arsenic release and methylation in paddy soil. Plant Soil 365:387–396CrossRefGoogle Scholar
  19. Jia Y, Huang H, Chen Z, Zhu YG (2014) Arsenic uptake by rice is influenced by microbe-mediated arsenic redox changes in the rhizosphere. Environ Sci Technol 48:1001–1007CrossRefGoogle Scholar
  20. Kaku N, Yonezawa N, Kodama Y, Watanabe K (2008) Plant/microbe cooperation for electricity generation in a rice paddy field. Appl Microbiol Biotechnol 79:43–49CrossRefGoogle Scholar
  21. Khudzari JM, Gariépy Y, Kurian J, Tartakovsky B, Raghavan GV (2019) Effects of biochar anodes in rice plant microbial fuel cells on the production of bioelectricity, biomass, and methane. Biochem Eng J 141:190–199CrossRefGoogle Scholar
  22. Kouzuma A, Kasai T, Nakagawa G, Yamamuro A, Abe T, Watanabe K (2013) Comparative metagenomics of anode-associated microbiomes developed in rice paddy-field microbial fuel cells. PLoS One 8:e77443CrossRefGoogle Scholar
  23. Kouzuma A, Kaku N, Watanabe K (2014) Microbial electricity generation in rice paddy fields: recent advances and perspectives in rhizosphere microbial fuel cells. Appl Microbiol Biotechnol 98:9521–9526CrossRefGoogle Scholar
  24. Li Y, Hu X, Yang S, Zhou J, Zhang T, Qi L, Sun X, Fan M, Xu S, Cha M (2017) Comparative analysis of the gut microbiota composition between captive and wild forest musk deer. Front Microbiol 8:1705CrossRefGoogle Scholar
  25. Li B, Zhou S, Wei D, Long J, Peng L, Tie B, Williams PN, Lei MJSTTE (2019) Mitigating arsenic accumulation in rice (Oryza sativa L.) from typical arsenic contaminated paddy soil of southern China using nanostructured α-MnO2: pot experiment and field application. Sci Total Environ 650:546–556CrossRefGoogle Scholar
  26. Liu WJ, Zhu YG, Smith F (2005) Effects of iron and manganese plaques on arsenic uptake by rice seedlings (Oryza sativa L.) grown in solution culture supplied with arsenate and arsenite. Plant Soil 277:127–138CrossRefGoogle Scholar
  27. Liu CW, Sung Y, Chen BC, Lai HY (2014) Effects of nitrogen fertilizers on the growth and nitrate content of lettuce (Lactuca sativa L.). Int J Environ Res Public Health 11:4427–4440CrossRefGoogle Scholar
  28. Liu B, Ji M, Zhai H (2018) Anodic potentials, electricity generation and bacterial community as affected by plant roots in sediment microbial fuel cell: effects of anode locations. Chemosphere 209:739–747Google Scholar
  29. Lovley DR (2017) Electrically conductive pili: biological function and potential applications in electronics. Curr Opin Electrochem 4:190–198CrossRefGoogle Scholar
  30. Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235CrossRefGoogle Scholar
  31. Malasarn D, Saltikov C, Campbell K, Santini J, Hering J, Newman D (2004) arrA is a reliable marker for As (V) respiration. Science 306:455–455CrossRefGoogle Scholar
  32. Mirza BS, Muruganadam S, Meng X, Sorensen DL, Dupont RR, McLean JE (2014) Arsenic (V) reduction in relation to iron (III) transformation and molecular characterization of the structural and functional microbial community in sediments of a basin-fill aquifer in Northern Utah. Appl Environ Microbiol 80(10):3198–3208Google Scholar
  33. Patel KS, Shrivas K, Brandt R, Jakubowski N, Corns W, Hoffmann P (2005) Arsenic contamination in water, soil, sediment and rice of Central India. Environ Geochem Health 27(2):131–145CrossRefGoogle Scholar
  34. Postma D, Jessen S, Hue NTM, Duc MT, Koch CB, Viet PH, Nhan PQ, Larsen F (2010) Mobilization of arsenic and iron from Red River floodplain sediments, Vietnam. Geochim Cosmochim Acta 74:3367–3381CrossRefGoogle Scholar
  35. Qiao JT, Li X, Li FB (2017a) Roles of different active metal-reducing bacteria in arsenic release from arsenic-contaminated paddy soil amended with biochar. J Hazard Mater 344:958–967CrossRefGoogle Scholar
  36. Qiao J, Li X, Hu M, Li F, Young LY, Sun W, Huang W, Cui J (2017b) Transcriptional activity of arsenic-reducing bacteria and genes regulated by lactate and biochar during arsenic transformation in flooded paddy soil. Environ Sci Technol 52:61–70CrossRefGoogle Scholar
  37. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2012) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596CrossRefGoogle Scholar
  38. Radloff KA, Cheng Z, Rahman MW, Ahmed KM, Mailloux BJ, Juhl AR, Schlosser P, van Geen A (2007) Mobilization of arsenic during one-year incubations of grey aquifer sands from Araihazar, Bangladesh. Environ Sci Technol 41:3639–3645CrossRefGoogle Scholar
  39. Rahman MA, Hasegawa H, Rahman MM, Rahman MA, Miah M (2007) Accumulation of arsenic in tissues of rice plant (Oryza sativa L.) and its distribution in fractions of rice grain. Chemosphere 69:942–948CrossRefGoogle Scholar
  40. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101CrossRefGoogle Scholar
  41. Sahrawat K (2005) Iron toxicity in wetland rice and the role of other nutrients. J Plant Nutr Soil Sci 27:1471–1504Google Scholar
  42. Schamphelaire LD, LVd B, Dang HS, Höfte M, Boon N, Rabaey K, Verstraete W (2008) Microbial fuel cells generating electricity from Rhizodeposits of rice plants. Environ Sci Technol 42:3053–3058CrossRefGoogle Scholar
  43. Seyfferth AL, McCurdy S, Schaefer MV, Fendorf S (2014) Arsenic concentrations in paddy soil and rice and health implications for major rice-growing regions of Cambodia. Environ Sci Technol 48(9):4699–4706CrossRefGoogle Scholar
  44. Slyemi D, Bonnefoy V (2012) How prokaryotes deal with arsenic. Environ Microbiol Rep 4:571–586Google Scholar
  45. Song N, Jiang HL (2018) Effects of initial sediment properties on start-up times for sediment microbial fuel cells. Int J Hydrog Energy 43(21):10082–10093CrossRefGoogle Scholar
  46. Stuckey Jason W, Schaefer Michael V, Kocar Benjamin D, Benner Shawn G, Fendorf S (2015) Arsenic release metabolically limited to permanently water-saturated soil in Mekong Delta. Nat Geosci 9:70–76CrossRefGoogle Scholar
  47. Sun Y, Polishchuk EA, Radoja U, Cullen WR (2004) Identification and quantification of arsC genes in environmental samples by using real-time PCR. J Microbiol Methods 58:335–349CrossRefGoogle Scholar
  48. Suriyagoda LD, Dittert K, Lambers H (2018) Mechanism of arsenic uptake, translocation and plant resistance to accumulate arsenic in rice grains. Agric Ecosyst Environ 253:23–37CrossRefGoogle Scholar
  49. Suzuki Y, Shimoda Y, Endo Y, Hata A, Yamanaka K, Endo G (2009) Rapid and effective speciation analysis of arsenic compounds in human urine using anion-exchange columns in HPLC-ICP-MS. J Occup Health Psychol 51:380–385CrossRefGoogle Scholar
  50. Takahashi Y, Minamikawa R, Hattori K, Kurishima K, Kihou N, Yuita K (2004) Arsenic behavior in paddy fields during the cycle of flooded and non-flooded periods. Environ Sci Technol 38:1038–1044CrossRefGoogle Scholar
  51. Takanezawa K, Nishio K, Kato S, Hashimoto K, Watanabe K (2010) Factors affecting electric output from rice-paddy microbial fuel cells. Biosci Biotechnol Biochem 74(6):1271–1273CrossRefGoogle Scholar
  52. Villegas-Torres MF, Bedoya-Reina OC, Salazar C, Vives-Florez MJ, Dussan J (2011) Horizontal arsC gene transfer among microorganisms isolated from arsenic polluted soil. Int Biodeterior Biodegradation 65:147–152CrossRefGoogle Scholar
  53. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefGoogle Scholar
  54. Wang N, Chen Z, Li HB, Su JQ, Zhao F, Zhu YG (2015) Bacterial community composition at anodes of microbial fuel cells for paddy soils: the effects of soil properties. J Soils Sediments 15:926–936CrossRefGoogle Scholar
  55. 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 16:1745–1753CrossRefGoogle Scholar
  56. Wang N, Xue X, Juhasz AL, Chang Z, Li H (2017) Biochar increases arsenic release from an anaerobic paddy soil due to enhanced microbial reduction of iron and arsenic. Environ Pollut 220:514–522CrossRefGoogle Scholar
  57. Wang X, Li F, Yuan C, Li B, Liu T, Liu C, Du Y, Liu C (2019a) The translocation of antimony in soil-rice system with comparisons to arsenic: alleviation of their accumulation in rice by simultaneous use of Fe (II) and NO3. Sci Total Environ 650:633–641CrossRefGoogle Scholar
  58. Wang M, Tang Z, Chen XP, Wang X, Zhou WX, Tang Z, Zhang J, Zhao FJ (2019b) Water management impacts the soil microbial communities and total arsenic and methylated arsenicals in rice grains. Environ Pollut 247:736–744CrossRefGoogle Scholar
  59. Wenzel WW, Kirchbaumer N, Prohaska T, Stingeder G, Lombi E, Adriano DC (2001) Arsenic fractionation in soils using an improved sequential extraction procedure. Anal Chim Acta 436(2):309–323CrossRefGoogle Scholar
  60. Williams PN, Zhang H, Davison W, Meharg AA, Hossain M, Norton GJ, Brammer H, Islam MR (2011) Organic matter solid phase interactions are critical for predicting arsenic release and plant uptake in Bangladesh Paddy soils. Environ Sci Technol 45:6080–6087CrossRefGoogle Scholar
  61. Wu M, Xu X, Lu K, Li X (2018) Effects of the presence of nanoscale zero-valent iron on the degradation of polychlorinated biphenyls and total organic carbon by sediment microbial fuel cell. Sci Total Environ 656:39–44CrossRefGoogle Scholar
  62. Yamaguchi N, Nakamura T, Dong D, Takahashi Y, Amachi S, Makino T (2011) Arsenic release from flooded paddy soils is influenced by speciation, Eh, pH, and iron dissolution. Chemosphere 83:925–932CrossRefGoogle Scholar
  63. Yamamura S, Sudo T, Watanabe M, Tsuboi S, Soda S, Ike M, Amachi S (2018) Effect of extracellular electron shuttles on arsenic-mobilizing activities in soil microbial communities. J Hazard Mater 342:571–578CrossRefGoogle Scholar
  64. Yang Y, Zhang H, Yuan H, Duan G, Jin D, Zhao F, Zhu Y (2018) Microbe mediated arsenic release from iron minerals and arsenic methylation in rhizosphere controls arsenic fate in soil-rice system after straw incorporation. Environ Pollut 236:598–608CrossRefGoogle Scholar
  65. You J, Wu G, Ren F, Chang Q, Yu B, Xue Y, Mu B (2016) Microbial community dynamics in Baolige oilfield during MEOR treatment, revealed by Illumina MiSeq sequencing. Appl Microbiol Biotechnol 100:1469–1478CrossRefGoogle Scholar
  66. Zhang SY, Zhao FJ, Sun G-X, Su J-Q, Yang XR, Li H, Zhu YG (2015) Diversity and abundance of arsenic biotransformation genes in paddy soils from southern China. Environ Sci Technol 49:4138–4146CrossRefGoogle Scholar
  67. Zhang J, Zhao S, Xu Y, Zhou W, Huang K, Tang Z, Zhao F-J (2017) Nitrate stimulates anaerobic microbial arsenite oxidation in paddy soils. Environ Sci Technol 51:4377–4386CrossRefGoogle Scholar
  68. Zhang J, Ma T, Yan Y, Xie X, Abass OK, Liu C, Zhao Z, Wang Z (2018) Effects of Fe-S-As coupled redox processes on arsenic mobilization in shallow aquifers of Datong Basin, northern China. Environ Pollut 237:28–38CrossRefGoogle Scholar
  69. Zhao FJ, Harris E, Yan J, Ma J, Wu L, Liu W, McGrath SP, Zhou J, Zhu YG (2013) Arsenic methylation in soils and its relationship with microbial arsM abundance and diversity, and As speciation in rice. Environ Sci Technol 47(13):7147–7154CrossRefGoogle Scholar
  70. Zhu YG, Sun GX, Lei M, Teng M, Liu YX, Chen NC, Wang LH, Carey A, Deacon C, Raab A (2008) High percentage inorganic arsenic content of mining impacted and nonimpacted Chinese rice. Environ Sci Technol 42:5008–5013CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Health and Environmental SciencesXi’an Jiaotong-Liverpool UniversitySuzhouChina
  2. 2.Department of Environmental ScienceUniversity of LiverpoolLiverpoolUK
  3. 3.Department of Biological SciencesXi’an Jiaotong-Liverpool UniversitySuzhouChina
  4. 4.Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, College of Resources and Environmental SciencesNanjing Agricultural UniversityNanjingChina

Personalised recommendations