Microbial community composition and electricity generation in cattle manure slurry treatment using microbial fuel cells: effects of inoculum addition

Abstract

Microbial fuel cell (MFC) is a sustainable technology to treat cattle manure slurry (CMS) for converting chemical energy to bioelectricity. In this work, two types of allochthonous inoculum including activated sludge (AS) and domestic sewage (DS) were added into the MFC systems to enhance anode biofilm formation and electricity generation. Results indicated that MFCs (AS + CMS) obtained the maximum electricity output with voltage approaching 577 ± 7 mV (~ 196 h), followed by MFCs (DS + CMS) (520 ± 21 mV, ~ 236 h) and then MFCs with autochthonous inoculum (429 ± 62 mV, ~ 263.5 h). Though the raw cattle manure slurry (RCMS) could facilitate electricity production in MFCs, the addition of allochthonous inoculum (AS/DS) significantly reduced the startup time and enhanced the output voltage. Moreover, the maximum power (1.259 ± 0.015 W/m2) and the highest COD removal (84.72 ± 0.48%) were obtained in MFCs (AS + CMS). With regard to microbial community, Illumina HiSeq of the 16S rRNA gene was employed in this work and the exoelectrogens (Geobacter and Shewanella) were identified as the dominant members on all anode biofilms in MFCs. For anode microbial diversity, the MFCs (AS + CMS) outperformed MFCs (DS + CMS) and MFCs (RCMS), allowing the occurrence of the fermentative (e.g., Bacteroides) and nitrogen fixation bacteria (e.g., Azoarcus and Sterolibacterium) which enabled the efficient degradation of the slurry. This study provided a feasible strategy to analyze the anode biofilm formation by adding allochthonous inoculum and some implications for quick startup of MFC reactors for CMS treatment.

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References

  1. Alsouleman K, Linke B, Klang J, Klocke M, Krakat N, Theuerl S (2016) Reorganisation of a mesophilic biogas microbiome as response to a stepwise increase of ammonium nitrogen induced by poultry manure supply. Bioresour Technol 208:200–204

    CAS  Article  Google Scholar 

  2. Ayyaru S, Dharmalingam S (2011) Development of MFC using sulphonated polyether ether ketone (SPEEK) membrane for electricity generation from waste water. Bioresour Technol 102:11167–11171

    CAS  Article  Google Scholar 

  3. Baranitharan E, Khan MR, Yousuf A, Teo WFA, Tan GYA, Cheng CK (2015) Enhanced power generation using controlled inoculum from palm oil mill effluent fed microbial fuel cell. Fuel 143:72–79

    CAS  Article  Google Scholar 

  4. Barker DJ, Stuckey DC (1999) A review of soluble microbial products (SMP) in wastewater treatment systems. Water Res 33:3063–3082

    CAS  Article  Google Scholar 

  5. Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555

    CAS  Article  Google Scholar 

  6. Bonmati A, Sotres A, Mu Y, Rozendal R, Rabaey K (2013) Oxalate degradation in a bioelectrochemical system: reactor performance and microbial community characterization. Bioresour Technol 143:147–153

    CAS  Article  Google Scholar 

  7. Catal T, Cysneiros D, O'Flaherty V, Leech D (2011) Electricity generation in single-chamber microbial fuel cells using a carbon source sampled from anaerobic reactors utilizing grass silage. Bioresour Technol 102:404–410

    CAS  Article  Google Scholar 

  8. Cerrillo M, Oliveras J, Vinas M, Bonmati A (2016) Comparative assessment of raw and digested pig slurry treatment in bioelectrochemical systems. Bioelectrochemistry 110:69–78

    CAS  Article  Google Scholar 

  9. Chae KJ, Choi MJ, Lee JW, Kim KY, Kim IS (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Bioresour Technol 100:3518–3525

    CAS  Article  Google Scholar 

  10. Chen W, Westerhoff P, ‡, JAL, §, Booksh‖ K (2003) Fluorescence excitation–emission matrix regional integration to quantify spectra for dissolved organic matter. Environ Sci Technol 37:5701–5710

  11. Cheng S, Xing D, Logan BE (2011) Electricity generation of single-chamber microbial fuel cells at low temperatures. Biosens Bioelectron 26:1913–1917

    CAS  Article  Google Scholar 

  12. Cheng HY, Liang B, Mu Y, Cui MH, Li K, Wu WM, Wang AJ (2015) Stimulation of oxygen to bioanode for energy recovery from recalcitrant organic matter aniline in microbial fuel cells (MFCs). Water Res 81:72–83

    CAS  Article  Google Scholar 

  13. Commault AS, Barriere F, Lapinsonniere L, Lear G, Bouvier S, Weld RJ (2015) Influence of inoculum and anode surface properties on the selection of Geobacter-dominated biofilms. Bioresour Technol 195:265–272

    CAS  Article  Google Scholar 

  14. Cui M-H, Cui D, Gao L, Cheng H-Y, Wang A-J (2016) Analysis of electrode microbial communities in an up-flow bioelectrochemical system treating azo dye wastewater. Electrochim Acta 220:252–257

    CAS  Article  Google Scholar 

  15. Dennis PG, Guo K, Imelfort M, Jensen P, Tyson GW, Rabaey K (2013) Spatial uniformity of microbial diversity in a continuous bioelectrochemical system. Bioresour Technol 129:599–605

    CAS  Article  Google Scholar 

  16. Ding A, Liang H, Qu F, Bai L, Li G, Ngo HH, Guo W (2014) Effect of granular activated carbon addition on the effluent properties and fouling potentials of membrane-coupled expanded granular sludge bed process. Bioresour Technol 171:240–246

    CAS  Article  Google Scholar 

  17. Dong Y, Qu Y, He W, Du Y, Liu J, Han X, Feng Y (2015) A 90-liter stackable baffled microbial fuel cell for brewery wastewater treatment based on energy self-sufficient mode. Bioresour Technol 195:66–72

    CAS  Article  Google Scholar 

  18. El-Chakhtoura J, El-Fadel M, Rao HA, Li D, Ghanimeh S, Saikaly PE (2014) Electricity generation and microbial community structure of air-cathode microbial fuel cells powered with the organic fraction of municipal solid waste and inoculated with different seeds. Biomass Bioenergy 67:24–31

    CAS  Article  Google Scholar 

  19. Fangueiro D, Hjorth M, Gioelli F (2015) Acidification of animal slurry—a review. J Environ Manag 149:46–56

    CAS  Article  Google Scholar 

  20. Ghadge AN, Jadhav DA, Pradhan H, Ghangrekar MM (2015) Enhancing waste activated sludge digestion and power production using hypochlorite as catholyte in clayware microbial fuel cell. Bioresour Technol 182:225–231

    CAS  Article  Google Scholar 

  21. Inoue K, Ito T, Kawano Y, Iguchi A, Miyahara M, Suzuki Y, Watanabe K (2013) Electricity generation from cattle manure slurry by cassette-electrode microbial fuel cells. J Biosci Bioeng 116:610–615

    CAS  Article  Google Scholar 

  22. Jia J, Tang Y, Liu B, Wu D, Ren N, Xing D (2013) Electricity generation from food wastes and microbial community structure in microbial fuel cells. Bioresour Technol 144:94–99

    CAS  Article  Google Scholar 

  23. Jung S, Regan JM (2007) Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors. Appl Microbiol Biotechnol 77:393–402

    CAS  Article  Google Scholar 

  24. Kiely PD, Cusick R, Call DF, Selembo PA, Regan JM, Logan BE (2011) Anode microbial communities produced by changing from microbial fuel cell to microbial electrolysis cell operation using two different wastewaters. Bioresour Technol 102:388–394

    CAS  Article  Google Scholar 

  25. Kim W, Shin SG, Han G, Cho K, Hwang S (2015) Structures of microbial communities found in anaerobic batch runs that produce methane from propionic acid—seeded from full-scale anaerobic digesters above a certain threshold. J Biotechnol 214:192–198

    CAS  Article  Google Scholar 

  26. Ledda C, Schievano A, Salati S, Adani F (2013) Nitrogen and water recovery from animal slurries by a new integrated ultrafiltration, reverse osmosis and cold stripping process: a case study. Water Res 47:6157–6166

    CAS  Article  Google Scholar 

  27. Li XM, Cheng KY, Selvam A, Wong JW (2013) Bioelectricity production from acidic food waste leachate using microbial fuel cells: effect of microbial inocula. Process Biochem 48:283–288

    CAS  Article  Google Scholar 

  28. Lin H, Wu X, Miller C, Zhu J (2013) Improved performance of microbial fuel cells enriched with natural microbial inocula and treated by electrical current. Biomass Bioenergy 54:170–180

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  30. Lu L, Xing D, Ren N (2012a) Bioreactor performance and quantitative analysis of methanogenic and bacterial community dynamics in microbial electrolysis cells during large temperature fluctuations. Environ Sci Technol 46:6874–6881

    CAS  Article  Google Scholar 

  31. Lu L, Xing D, Ren N (2012b) Pyrosequencing reveals highly diverse microbial communities in microbial electrolysis cells involved in enhanced H2 production from waste activated sludge. Water Res 46:2425–2434

    CAS  Article  Google Scholar 

  32. Lu L, Xing D, Ren ZJ (2015) Microbial community structure accompanied with electricity production in a constructed wetland plant microbial fuel cell. Bioresour Technol 195:115–121

    CAS  Article  Google Scholar 

  33. Mardanpour MM, Nasr Esfahany M, Behzad T, Sedaqatvand R (2012) Single chamber microbial fuel cell with spiral anode for dairy wastewater treatment. Biosens Bioelectron 38:264–269

    Article  Google Scholar 

  34. Masse DI, Saady NM (2015) High rate psychrophilic anaerobic digestion of undiluted dairy cow feces. Bioresour Technol 187:128–135

    CAS  Article  Google Scholar 

  35. Mei X, Guo C, Liu B, Tang Y, Xing D (2015) Shaping of bacterial community structure in microbial fuel cells by different inocula. RSC Adv 5:78136–78141

    CAS  Article  Google Scholar 

  36. Min B, Kim J, Oh S, Regan JM, Logan BE (2005) Electricity generation from swine wastewater using microbial fuel cells. Water Res 39:4961–4968

    CAS  Article  Google Scholar 

  37. Pasternak G, Greenman J, Ieropoulos I (2016) Regeneration of the power performance of cathodes affected by biofouling. Appl Energy 173:431–437

    CAS  Article  Google Scholar 

  38. Qu F, Liang H, He J, Ma J, Wang Z, Yu H, Li G (2012) Characterization of dissolved extracellular organic matter (dEOM) and bound extracellular organic matter (bEOM) of Microcystis aeruginosa and their impacts on UF membrane fouling. Water Res 46:2881–2890

    CAS  Article  Google Scholar 

  39. Ren L, Ahn Y, Logan BE (2014) A two-stage microbial fuel cell and anaerobic fluidized bed membrane bioreactor (MFC-AFMBR) system for effective domestic wastewater treatment. Environ Sci Technol 48:4199–4206

    CAS  Article  Google Scholar 

  40. Rismani-Yazdi H, Carver SM, Christy AD, Yu Z, Bibby K, Peccia J, Tuovinen OH (2013) Suppression of methanogenesis in cellulose-fed microbial fuel cells in relation to performance, metabolite formation, and microbial population. Bioresour Technol 129:281–288

    CAS  Article  Google Scholar 

  41. Saidu M, Yuzir A, Salim MR, Salmiati AS, Abdullah N (2013) Influence of palm oil mill effluent as inoculum on anaerobic digestion of cattle manure for biogas production. Bioresour Technol 141:174–176

    CAS  Article  Google Scholar 

  42. Scherr KE, Backes D, Scarlett AG, Lantschbauer W, Nahold M (2016) Biogeochemical gradients above a coal tar DNAPL. Sci Total Environ 563-564:741–754

    CAS  Article  Google Scholar 

  43. Sotres A, Cerrillo M, Vinas M, Bonmati A (2015) Nitrogen recovery from pig slurry in a two-chambered bioelectrochemical system. Bioresour Technol 194:373–382

    CAS  Article  Google Scholar 

  44. Sotres A, Tey L, Bonmati A, Vinas M (2016) Microbial community dynamics in continuous microbial fuel cells fed with synthetic wastewater and pig slurry. Bioelectrochemistry 111:70–82

    CAS  Article  Google Scholar 

  45. Sun R, Zhou A, Jia J, Liang Q, Liu Q, Xing D, Ren N (2015) Characterization of methane production and microbial community shifts during waste activated sludge degradation in microbial electrolysis cells. Bioresour Technol 175:68–74

    CAS  Article  Google Scholar 

  46. Tanikkul P, Pisutpaisal N (2015) Influence of inoculum pretreatment on the performance of an air-cathode single-chamber microbial fuel cell. Energy Procedia 79:641–645

    CAS  Article  Google Scholar 

  47. Toumi J, Miladi B, Farhat A, Nouira S, Hamdi M, Gtari M, Bouallagui H (2015) Microbial ecology overview during anaerobic codigestion of dairy wastewater and cattle manure and use in agriculture of obtained bio-fertilisers. Bioresour Technol 198:141–149

    Article  Google Scholar 

  48. Usack JG, Angenent LT (2015) Comparing the inhibitory thresholds of dairy manure co-digesters after prolonged acclimation periods: part 1—performance and operating limits. Water Res 87:446–457

    CAS  Article  Google Scholar 

  49. Velvizhi G, Mohan SV (2015) Bioelectrogenic role of anoxic microbial anode in the treatment of chemical wastewater: microbial dynamics with bioelectro-characterization. Water Res 70:52–63

    CAS  Article  Google Scholar 

  50. Xiao K, Zhou Y, Guo C, Maspolim Y, Ng WJ (2015) Dynamics of propionic acid degradation in a two-phase anaerobic system. Chemosphere 140:47–53

    CAS  Article  Google Scholar 

  51. Yu H, Qu F, Liang H, Z-s H, Ma J, Shao S, Chang H, Li G (2014) Understanding ultrafiltration membrane fouling by extracellular organic matter of Microcystis aeruginosa using fluorescence excitation–emission matrix coupled with parallel factor analysis. Desalination 337:67–75

    CAS  Article  Google Scholar 

  52. Yu J, Fan C, Zhong J, Zhang Y, Wang C, Zhang L (2016) Evaluation of in situ simulated dredging to reduce internal nitrogen flux across the sediment-water interface in Lake Taihu, China. Environ Pollut 214:866–877

    CAS  Article  Google Scholar 

  53. Zhang J, Zheng P, Zhang M, Chen H, Chen T, Xie Z, Cai J, Abbas G (2013) Kinetics of substrate degradation and electricity generation in anodic denitrification microbial fuel cell (AD-MFC). Bioresour Technol 149:44–50

    CAS  Article  Google Scholar 

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Acknowledgements

The authors would like to specially thank the supports by the Scientific and Research Foundation for Returned Scholars of Heilongjiang Province (LC2016015), the Young Talents Project of Northeast Agricultural University (14QC35), the Specialized Fund Project for Harbin Innovative Talent in Science and Technology Research (2013RFQXJ094), and the HIT Environment and Ecology Innovation Special Funds (HSCJ201603)

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Correspondence to Weijia Gong or Heng Liang.

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Highlights

1. Addition of allochthonous inocula (AS/DS) shortened the startup period in MFCs.

2. The MFCs with AS as allochthonous inocula exhibited the best performance.

3. Co-addition of AS enhanced the anode biofilm formation and diversity in MFCs.

4. The finding contributed to a quick startup of MFCs for CMS treatment.

Responsible editor: Diane Purchase

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Xie, B., Gong, W., Ding, A. et al. Microbial community composition and electricity generation in cattle manure slurry treatment using microbial fuel cells: effects of inoculum addition. Environ Sci Pollut Res 24, 23226–23235 (2017). https://doi.org/10.1007/s11356-017-9959-4

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Keywords

  • Microbial fuel cell (MFC)
  • Cattle manure slurry (CMS)
  • Microbial community structure
  • Inoculum
  • Startup time