Abstract
The effect of electricity, induced by external resistance, on microbial community performance is investigated in Microbial Fuel Cells (MFCs) involved in simultaneous biotransformation of sulfide and nitrate. In the experiment, three MFCs were operated under different external resistances (100 Ω, 1000 Ω and 10,000 Ω), while one MFC was operated with open circuit as control. All MFCs demonstrate good capacity for simultaneous sulfide and nitrate biotransformation regardless of external resistance. MFCs present similar voltage profile; however, the output voltage has positive relationship with external resistance, and the MFC1 with lowest external resistance (100 Ω) generated highest power density. High-throughput sequencing confirms that taxonomic distribution of suspended sludge in anode chamber encompass phylum level to genus level, while the results of principal component analysis (PCA) suggest that microbial communities are varied with external resistance, which external resistance caused the change of electricity generation and substrate removal at the same, and then leads to the change of microbial communities. However, based on Pearson correlation analyses, no strong correlation is evident between community diversity indices (ACE index, Chao index, Shannon index and Simpson index) and the electricity (final voltage and current density). It is inferred that the performance of electricity did not significantly affect the diversity of microbial communities in MFCs biotransforming sulfide and nitrate simultaneously.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ai T, Zhan H, Zou L, Fu J, Fu Q, He Q, Ai H (2020) Potential applications of endogenous sulfide for enhanced denitrification of low C/N domestic wastewater in anodic mixotrophic denitrification microbial fuel cell: the mechanism of electrons transfer and microbial community. Sci Tot Environ 722:137830. https://doi.org/10.1016/j.scitotenv.2020.137830
Amato KR et al (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J 7:1344. https://doi.org/10.1038/ismej.2013.16
APHA, AWWA, WPCF (1998) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington, DC
Blazquez E, Baeza JA, Gabriel D, Guisasola A (2019) Treatment of real flue gas desulfurization wastewater in an autotrophic biocathode in view of elemental sulfur recovery: microbial communities involved. Sci Tot Environ 657:945–952. https://doi.org/10.1016/j.scitotenv.2018.12.037
Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science (New York NY) 295:483–485. https://doi.org/10.1126/science.1066771
Cai J, Zheng P (2013) Simultaneous anaerobic sulfide and nitrate removal in microbial fuel cell. Bioresour Technol 128:760–764. https://doi.org/10.1016/j.biortech.2012.08.046
Cai J, Jiang J, Zheng P (2010) Isolation and identification of bacteria responsible for simultaneous anaerobic ammonium and sulfate removal. Science China Chem 53:645–650. https://doi.org/10.1007/s11426-010-0053-8
Cai J, Zheng P, Zhang J, Xie Z, Li W, Sun P (2013) Simultaneous anaerobic sulfide and nitrate removal coupled with electricity generation in microbial fuel. Cell Bioresour Technol 129:224–228. https://doi.org/10.1016/j.biortech.2012.11.008
Cai J, Zheng P, Qaisar M, Sun P (2014a) Effect of electrode types on simultaneous anaerobic sulfide and nitrate removal in microbial fuel cell. Sep Purif Technol 134:20–25. https://doi.org/10.1016/j.seppur.2014.07.024
Cai J, Zheng P, Qaisar M, Xing Y (2014b) Effect of operating modes on simultaneous anaerobic sulfide and nitrate removal in microbial fuel cell. J Ind Microbiol Biotechnol 41:795–802. https://doi.org/10.1007/s10295-014-1425-4
Cai J, Zheng P, Xing Y, Qaisar M (2015) Effect of electricity on microbial community of microbial fuel cell simultaneously treating sulfide and nitrate. J Power Sources 281:27–33
Cai J, Zheng P, Mahmood Q (2016) Effect of cathode electron acceptors on simultaneous anaerobic sulfide and nitrate removal in microbial fuel cell. Water Sci Technol 73:947
Dong ZS, Zhao Y, Fan L, Wang YX, Wang JW, Zhang K (2017) Simultaneous sulfide removal and hydrogen production in a microbial electrolysis. Cell Int J Electrochem Sci 12:10553–10566. https://doi.org/10.20964/2017.11.53
Eddie C, Jaap VR, Andreas S, Armin G, Dirk DB, Dror M (2005) Identification of bacteria potentially responsible for oxic and anoxic sulfide oxidation in biofilters of a recirculating mariculture system. Appl Environ Microbiol 71:6134–6141
Feng SS, Lin X, Tong YJ, Huang X, Yang HL (2018) Biodesulfurization of sulfide wastewater for elemental sulfur recovery by isolated Halothiobacillus neapolitanus in an internal airlift loop reactor. Bioresour Technol 264:244–252. https://doi.org/10.1016/j.biortech.2018.05.079
Garcia-de-Lomas J, Corzo A, Portillo MC, Gonzalez JM, Andrades JA, Saiz-Jimenez C, Garcia-Robledo E (2007) Nitrate stimulation of indigenous nitrate-reducing, sulfide-oxidising bacterial community in wastewater anaerobic biofilms. Water Res 41:3121–3131. https://doi.org/10.1016/j.watres.2007.04.004
Gil G-C, Chang I-S, Kim BH, Kim M, Jang J-K, Park HS, Kim HJ (2003) Operational parameters affecting the performannce of a mediator-less microbial fuel cell. Biosensors Bioelectron 18:327–334. https://doi.org/10.1016/S0956-5663(02)00110-0
Habermann W, Pommer EH (1991) Biological fuel cells with sulphide storage capacity. Appl Microbiol Biotechnol 35:128–133
Hu Z, Lu X, Sun P, Hu Z, Wang R, Lou C, Han J (2017) Understanding the performance of microbial community induced by ZnO nanoparticles in enhanced biological phosphorus removal system and its recoverability. Bioresour Technol 225:279–285. https://doi.org/10.1016/j.biortech.2016.11.080
Huang L, Li X, Cai T, Huang M (2018) Electrochemical performance and community structure in three microbial fuel cells treating landfill leachate Process. Saf Environ Prot 113:378–387. https://doi.org/10.1016/j.psep.2017.11.008
Ieropoulos I, Greenman J, Melhuish C, Hart J (2005) Energy accumulation and improved performance in microbial fuel cells. J Power Sources 145:253–256. https://doi.org/10.1016/j.jpowsour.2004.11.070
Ieropoulos I, Melhuish C, Greenman J (2007) Artificial gills for robots: MFC behaviour in water. Bioinspir Biomim 2:S83–S93. https://doi.org/10.1088/1748-3182/2/3/s02
Jiang C et al (2017) Simultaneous perchlorate and nitrate removal coupled with electricity generation in autotrophic denitrifying biocathode microbial fuel cell. Chem Eng J 308:783–790. https://doi.org/10.1016/j.cej.2016.09.121
Kondaveeti S, Lee S-H, Park H-D, Min B (2014) Bacterial communities in a bioelectrochemical denitrification system: the effects of supplemental electron acceptors. Water Res 51:25–36. https://doi.org/10.1016/j.watres.2013.12.023
Kostrytsia A, Papirio S, Morrison L, Ijaz UZ, Collins G, Lens PNL, Esposito G (2018) Biokinetics of microbial consortia using biogenic sulfur as a novel electron donor for sustainable denitrification. Bioresour Technol 270:359–367. https://doi.org/10.1016/j.biortech.2018.09.044
Kumar SS et al (2019) Microbial fuel cells (MFCs) for bioelectrochemical treatment of different wastewater streams. Fuel 254:115526. https://doi.org/10.1016/j.fuel.2019.05.109
Lee CY, Ho KL, Lee DJ, Su A, Chang JS (2012) Electricity harvest from nitrate/sulfide-containing wastewaters using microbial fuel cell with autotrophic denitrifier, Pseudomonas sp. C27. Int J Hydrog Energy 37:15827–15832. https://doi.org/10.1016/j.ijhydene.2012.01.092
Li M, Zhou M, Tian X, Tan C, McDaniel CT, Hassett DJ, Gu T (2018) Microbial fuel cell (MFC) power performance improvement through enhanced microbial electrogenicity. Biotechnol Adv 36:1316–1327. https://doi.org/10.1016/j.biotechadv.2018.04.010
Lin S, Mackey HR, Hao T, Guo G, van Loosdrecht MCM, Chen G (2018) Biological sulfur oxidation in wastewater treatment: a review of emerging opportunities. Water Res 143:399–415. https://doi.org/10.1016/j.watres.2018.06.051
Logan BE et al (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40:5181–5192. https://doi.org/10.1021/es0605016
Lyon DY, Buret F, Vogel TM, Monier J-M (2010) Is resistance futile? Changing external resistance does not improve microbial fuel cell performance . Bioelectrochemistry 78:2–7. https://doi.org/10.1016/j.bioelechem.2009.09.001
Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton
Mahmood Q, Zheng P, Cai J, Wu D, Hu B, Li J (2007) Anoxic sulfide biooxidation using nitrite as electron acceptor. J Hazard Mater 147:249–256. https://doi.org/10.1016/j.jhazmat.2007.01.002
Mahmood Q, Hu BL, Cai J, Zheng P, Azim MR, Jilani G, Islam E (2009) Isolation of Ochrobactrum sp. QZ2 from sulfide and nitrite treatment system. J Hazard Mater 165:558–565. https://doi.org/10.1016/j.jhazmat.2008.10.021
Mateo S, Cañizares P, Rodrigo MA, Fernández-Morales FJ (2019) Reproducibility and robustness of microbial fuel cells technology. J Power Sources 412:640–647. https://doi.org/10.1016/j.jpowsour.2018.12.007
Mestrinelli F, Pozzi E, Sakamoto IK, Foresti E (2016) Isolation and characterization of a microorganism involved in sulfide-oxidizing autotrophic denitrification in a vertical fixed-bed reactor. J Water Process Eng 11:138–142. https://doi.org/10.1016/j.jwpe.2016.04.003
Montebello AM et al (2013) Operational aspects, pH transition and microbial shifts of a H2S desulfurizing biotrickling filter with random packing. Mater Chemosphere 93:2675–2682. https://doi.org/10.1016/j.chemosphere.2013.08.052
Pasternak G, Greenman J, Ieropoulos I (2018) Dynamic evolution of anodic biofilm when maturing under different external resistive loads in microbial fuel cells. Electrochem Perspect J Power Sources 400:392–401. https://doi.org/10.1016/j.jpowsour.2018.08.031
Pinto RP, Srinivasan B, Guiot SR, Tartakovsky B (2011) The effect of real-time external resistance optimization on microbial fuel cell performance. Water Res 45:1571–1578. https://doi.org/10.1016/j.watres.2010.11.033
Poirier S, Madigou C, Bouchez T, Chapleur O (2017) Improving anaerobic digestion with support media: mitigation of ammonia inhibition and effect on microbial communities. Bioresour Technol 235:229–239. https://doi.org/10.1016/j.biortech.2017.03.099
Pokorna D, Zabranska J (2015) Sulfur-oxidizing bacteria in environmental technology. Biotechnol Adv 33:1246–1259. https://doi.org/10.1016/j.biotechadv.2015.02.007
Rago L, Monpart N, Cortes P, Baeza JA, Guisasola A (2016) Performance of microbial electrolysis cells with bioanodes grown at different external resistances. Water Sci Technol 73:1129–1135. https://doi.org/10.2166/wst.2015.418
Rismani-Yazdi H, Christy AD, Carver SM, Yu Z, Dehority BA, Tuovinen OH (2011) Effect of external resistance on bacterial diversity and metabolism in cellulose-fed microbial fuel cells. Bioresour Technol 102:278–283. https://doi.org/10.1016/j.biortech.2010.05.012
Sangcharoen A, Niyom W, Suwannasilp BB (2015) A microbial fuel cell treating organic wastewater containing high sulfate under continuous operation: performance and microbial community. Process Biochem 50:1648–1655. https://doi.org/10.1016/j.procbio.2015.06.013
Shi J et al (2018) Enhanced performance of sediment microbial fuel cell by immobilization of Shewanella oneidensis MR-1 on an anode surface. Int J Hydrog Energy. https://doi.org/10.1016/j.ijhydene.2018.11.225
Sotres A, Cerrillo M, Viñas M, Bonmatí A (2015) Nitrogen recovery from pig slurry in a two-chambered bioelectrochemical system. Bioresour Technol 194:373–382. https://doi.org/10.1016/j.biortech.2015.07.036
Sotres A, Tey L, Bonmatí A, Viñas M (2016) Microbial community dynamics in continuous microbial fuel cells fed with synthetic wastewater and pig slurry. Bioelectrochemistry 111:70–82. https://doi.org/10.1016/j.bioelechem.2016.04.007
Sun M et al (2010) Microbial communities involved in electricity generation from sulfide oxidation in a microbial fuel cell. Biosens Bioelectron 26:470–476. https://doi.org/10.1016/j.bios.2010.07.074
Suzuki K et al (2018) Bacterial communities adapted to higher external resistance can reduce the onset potential of anode in microbial fuel cells. J Biosci Bioeng 125:565–571. https://doi.org/10.1016/j.jbiosc.2017.12.018
Wan R, Wang L, Chen YG, Zheng X, Su YL, Tao XC (2018) Insight into a direct carbon dioxide effect on denitrification and denitrifying bacterial communities in estuarine sediment. Sci Tot Environ 643:1074–1083. https://doi.org/10.1016/j.scitotenv.2018.06.279
Wang X, Zhang Y, Zhang T, Zhou J (2016) Effect of dissolved oxygen on elemental sulfur generation in sulfide and nitrate removal process: characterization, pathway, and microbial community analysis. Appl Microbiol Biotechnol 100:2895–2905. https://doi.org/10.1007/s00253-015-7146-4
Wang K, Zhang S, Chen Z, Bao R (2018) Interactive effect of electrode potential on pollutants conversion in denitrifying sulfide removal microbial fuel cells. Chem Eng J 339:442–449. https://doi.org/10.1016/j.cej.2018.01.114
Wang W et al (2020) Operation mechanism of constructed wetland-microbial fuel cells for wastewater treatment and electricity generation. A review. Bioresour Technol 314:123808. https://doi.org/10.1016/j.biortech.2020.123808
Watsuntorn W, Ruangchainikom C, Rene ER, Lens PNL, Chulalaksananukul W (2019) Comparison of sulphide and nitrate removal from synthetic wastewater by pure and mixed cultures of nitrate-reducing sulphide-oxidizing bacteria. Bioresour Technol 272:40–47. https://doi.org/10.1016/j.biortech.2018.09.125
Xia T et al (2019) Power generation and microbial community analysis in microbial fuel cells: a promising system to treat organic acid fermentation wastewater. Bioresour Technol. https://doi.org/10.1016/j.biortech.2019.03.119
Yang N, Zhan G, Li D, Wang X, He X, Liu H (2019) Complete nitrogen removal and electricity production in Thauera-dominated air-cathode single chambered microbial fuel cell. Chem Eng J 356:506–515. https://doi.org/10.1016/j.cej.2018.08.161
Zhang B et al (2013) Identification of removal principles and involved bacteria in microbial fuel cells for sulfide removal and electricity generation. Int J Hydrog Energy 38:14348–14355. https://doi.org/10.1016/j.ijhydene.2013.08.131
Zhi W, Ge Z, He Z, Zhang H (2014) Methods for understanding microbial community structures and functions in microbial fuel cells. A review . Bioresour Technol 171:461–468. https://doi.org/10.1016/j.biortech.2014.08.096
Acknowledgements
This work was supported by the National Natural Science Foundation of China [51808494], Zhejiang Provincial Natural Science Foundation of China [LY18E080007], the Scientific Research Fund of Zhejiang Provincial Education Department [Y201635678] and the Project of Shandong Province Higher Educational Science and Technology Program [J16LD03].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cai, J., Qaisar, M., Ding, A. et al. Insights into microbial community in microbial fuel cells simultaneously treating sulfide and nitrate under external resistance. Biodegradation 32, 73–85 (2021). https://doi.org/10.1007/s10532-021-09926-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-021-09926-1