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Dynamic changes in the microbial community composition in microbial fuel cells fed with sucrose

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Abstract

The performance and dynamics of the bacterial communities in the biofilm and suspended culture in the anode chamber of sucrose-fed microbial fuel cells (MFCs) were studied by using denaturing gradient gel electrophoresis (DGGE) of PCR-amplified partial 16S rRNA genes followed by species identification by sequencing. The power density of MFCs was correlated to the relative proportions of species obtained from DGGE analysis in order to detect bacterial species or taxonomic classes with important functional role in electricity production. Although replicate MFCs showed similarity in performance, cluster analysis of DGGE profiles revealed differences in the evolution of bacterial communities between replicate MFCs. No correlation was found between the proportion trends of specific species and the enhancement of power output. However, in all MFCs, putative exoelectrogenic denitrifiers and sulphate-reducers accounted for approximately 24% of the bacterial biofilm community at the end of the study. Pareto–Lorenz evenness distribution curves extracted from the DGGE patterns obtained from time course samples indicated community structures where shifts between functionally similar species occur, as observed within the predominant fermentative bacteria. These results suggest the presence of functional redundancy within the anodic communities, a probable indication that stable MFC performance can be maintained in changing environmental conditions. The capability of bacteria to adapt to electricity generation might be present among a wide range of bacteria.

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References

  • Aelterman P, Rabaey K, Pham HT, Boon N, Verstraete W (2006) Continuous electricity generation at high voltages and currents using stacked microbial fuel cells. Environ Sci Technol 40:3388–3394

    Article  CAS  Google Scholar 

  • Aelterman P, Rabaey K, de Schamphelaire L, Clauwaert P, Boon N, Verstraete W (2008a) Microbial fuel cells as an engineered ecosystem. In: Wall JD, Harwood CS, Demain AL (eds) Bioenergy. ASM, Washington, pp 307–320

    Google Scholar 

  • Aelterman P, Versichele M, Marzorati M, Boon N, Verstraete W (2008b) Loading rate and external resistance control the electricity generation of microbial fuel cells with different three-dimensional anodes. Biores Technol 99:8895–8902

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Borole AP, Hamilton CY, Vishnivetskaya TA, Leak D, Andras C, Morrell-Falvey J, Keller M, Davison B (2009) Integrating engineering design improvements with exoelectrogen enrichment process to increase power output from microbial fuel cells. J Power Sour 191:520–527

    Article  CAS  Google Scholar 

  • Bretschger O, Obraztsova A, Sturm CA, Chang IS, Gorby YA, Reed SB, Culley DE, Reardon CL, Barua S, Romine MF, Zhou J, Beliaev AS, Bouhenni R, Saffarini D, Mansfeld F, Kim BH, Fredrickson JK, Nealson KH (2007) Current production and metal oxide reduction by Shewanella oneidensis MR-1 wild type and mutants. Appl Environ Microbiol 73:7003–7012

    Article  CAS  Google Scholar 

  • Briones A, Raskin L (2003) Diversity and dynamics of microbial communities in engineered environments and their implications for process stability. Curr Opin Biotechnol 14:270–276

    Article  CAS  Google Scholar 

  • Chae KJ, Choi M-J, Lee J-W, Kim KY, Kim IS (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Biores Technol 100:3518–3525

    Article  CAS  Google Scholar 

  • Chaudhuri SK, Lovley DR (2003) Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nat Biotechnol 21:1229–1232

    Article  CAS  Google Scholar 

  • Choo YF, Lee J, Chang IS, Kim BH (2006) Bacterial communities in microbial fuel cells enriched with high concentrations of glucose and glutamate. J Microbiol Biotechnol 16:1481–1484

    CAS  Google Scholar 

  • Chung K, Okabe S (2009) Continuous power generation and microbial community structure of the anode biofilms in a three-stage microbial fuel cell system. Appl Microbiol Biotechnol 83:965–977

    Article  CAS  Google Scholar 

  • Curtis TP, Sloan WT (2004) Prokaryotic diversity and its limits: microbial community structure in nature and implications for microbial ecology. Curr Opin Microbiol 7:221–226

    Article  Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith S (1956) Colorimetric method for the determination of sugars and related substances. Analyt Chem 28:350–356

    Article  CAS  Google Scholar 

  • El Fantroussi S, Verschuere L, Verstraete W, Top EM (1999) Effect of phenylurea herbicides on soil microbial communities estimated by analysis of 16S rRNA gene fingerprints and community-level physiological profiles. Appl Environ Microbiol 65:982–988

    CAS  Google Scholar 

  • Fedorovich V, Knighton MC, Pagaling E, Ward FB, Free A, Goryanin I (2009) A novel electrochemically active bacterium phylogenetically related to Arcobacter butzleri isolated from a microbial fuel cell. Appl Environ Microbiol 75:7326–7334

    Article  CAS  Google Scholar 

  • Fernández A, Hashsham SA, Dollhopf SL, Raskin L, Glagoleva O, Dazzo FB, Hickey RF, Criddle CS, Tiedje JM (2000) Flexible community structure correlates with stable community function in methanogenic bioreactor communities perturbed by glucose. Appl Environ Microbiol 66:4058–4067

    Article  Google Scholar 

  • Frias-Lopez J, Shi Y, Tyson GW, Coleman ML, Schuster SC, Chisholm SW, DeLong EF (2008) Microbial community gene expression in ocean surface waters. Proc Natl Acad Sci 105:3805–3810

    Article  CAS  Google Scholar 

  • Fromin N, Hamelin J, Tarnawski S, Roesti D, Jourdain-Miserez K, Forestier N, Teyssier-Cuvelle S, Gillet F, Aragno M, Rossi P (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4:634–643

    Article  CAS  Google Scholar 

  • Gafan GP, Spratt DA (2005) Denaturing gradient gel electrophoresis gel expansion (DGGEGE)—an attempt to resolve the limitations of co-migration in the DGGE of complex polymicrobial communities. FEMS Microbiol Lett 253:303–307

    Article  CAS  Google Scholar 

  • Gentile ME, Nyman JL, Criddle CS (2007) Correlation of patterns of denitrification instability in replicated bioreactor communities with shifts in the relative abundance and the denitrification patterns of specific populations. ISME J 1:714–728

    Article  CAS  Google Scholar 

  • Green SJ (2006) A guide to denaturing gradient gel electrophoresis. Available at http://ddgehelp.blogspot.com/. Accessed 17 March 2011

  • Green SJ, Leigh MB, Neufeld JD (2009) Denaturing gradient gel electrophoresis (DGGE) for microbial community analysis. In: Timmis KN (ed) Microbiology of hydrocarbons, oils, lipids and derived compounds. Springer, Heidelberg, pp 4137–4158

    Google Scholar 

  • Gumaelius L, Magnusson G, Pettersson B, Dalhammar G (2001) Comamonas denitrificans sp. nov., an efficient denitrifying bacterium isolated from activated sludge. Int J Syst Evol Microbiol 51:999–1006

    Article  CAS  Google Scholar 

  • He Z, Minteer SD, Angenent LT (2005) Electricity generation from artificial wastewater using an upflow microbial fuel cell. Environ Sci Technol 39:5262–5267

    Article  CAS  Google Scholar 

  • Holt JG (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams & Wilkins, Baltimore

    Google Scholar 

  • Ieropoulos I, Greenman J, Melhuish C (2008) Microbial fuel cells based on carbon veil electrodes: Stack configuration and scalability. Int J Energy Res 32:1228–1240

    Article  CAS  Google Scholar 

  • Jeong JG, Lim YW, Yi H, Sekiguchi Y, Kamagata Y, Chun J (2007) Anaerosporobacter mobilis gen. nov., sp. nov., isolated from forest soil. Int J Syst Evol Microbiol 57:1784–1787

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kaewpipat K, Grady CPL (2002) Microbial population dynamics in laboratory-scale activated sludge reactors. Water Sci Technol 46:19–27

    CAS  Google Scholar 

  • Katuri KP, Scott K, Head IM, Picioreanu C, Curtis TP (2011) Microbial fuel cells meet with external resistance. Biores Technol 102:2758–2766

    Article  CAS  Google Scholar 

  • Kim JR, Cheng S, Oh S-E, Logan BE (2007) Power generation using different cation, anion, and ultrafiltration membranes in microbial fuel cells. Environ Sci Technol 41:1004–1009

    Article  CAS  Google Scholar 

  • Kim JR, Beecroft NJ, Varcoe JR, Dinsdale RM, Guwy AJ, Thumser AE, Slade RCT, Avignone-Rossa C, Premier GC (2011) Spatio-temporal development of the bacterial community in a tubular longitudinal microbial fuel cell. Appl Microbiol Biotechnol 90:1179–1191

    Article  CAS  Google Scholar 

  • Koskinen PEP, Kaksonen AH, Puhakka JA (2007) The relationship between instability of H2 production and compositions of bacterial communities within a dark fermentation fluidised-bed bioreactor. Biotechnol Bioeng 97:742–758

    Article  CAS  Google Scholar 

  • Lawson PA, Falsen E, Inganäs E, Weyant RS, Collins MD (2002) Dysgonomonas mossii sp. nov., from human sources. System Appl Microbiol 25:194–197

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lorenz MO (1905) Methods of measuring concentration of wealth. J Am Stat Assoc 9:209–219

    Google Scholar 

  • Lovley DR, Greening RC, Ferry JG (1984) Rapidly growing rumen methanogenic organism that synthesizes coenzyme M and has a high affinity for formate. Appl Environ Microbiol 48:81–87

    CAS  Google Scholar 

  • Marzorati M, Wittebolle L, Boon N, Daffonchio D, Verstraete W (2008) How to get more out of molecular fingerprints: practical tools for microbial ecology. Environ Microbiol 10:1571–1581

    Article  CAS  Google Scholar 

  • Mehanna M, Kiely PD, Call DF, Logan B (2010) Microbial electrodialysis cell for simultaneous water desalination and hydrogen gas production. Environ Sci Technol 44:9578–9583

    Article  CAS  Google Scholar 

  • Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Anton van Leeuwen 73:127–141

    Article  CAS  Google Scholar 

  • Nishiyama T, Ueki A, Kaku N, Watanabe K, Ueki K (2009) Bacteroides graminisolvens sp. nov., a xylanolytic anaerobe isolated from a methanogenic reactor treating cattle waste. Int J Syst Evol Microbiol 59:1901–1907

    Article  CAS  Google Scholar 

  • Pham TH, Boon N, Aelterman P, Clauwaert P, de Schamphelaire L, Vanhaecke L, De Maeyer K, Höfte M, Verstraete W, Rabaey K (2008) Metabolites produced by Pseudomonas sp. enable a Gram-positive bacterium to achieve extracellular electron transfer. Appl Microbiol Biotechnol 77:1119–1129

    Article  CAS  Google Scholar 

  • Pham TH, Aelterman P, Verstraete W (2009) Bioanode performance in bioelectrochemical systems: recent improvements and prospects. Trends Biotechnol 27:168–178

    Article  CAS  Google Scholar 

  • Phung NT, Lee J, Kang KH, Chang IS, Gadd GM, Kim BH (2004) Analysis of microbial diversity in oligotrophic microbial fuel cells using 16S rDNA sequences. FEMS Microbiol Lett 233:77–82

    Article  CAS  Google Scholar 

  • Rabaey K, Rozendal RA (2010) Microbial electrosynthesis—revisiting the electrical route for microbial production. Nat Rev Micro 8:706–716

    Article  CAS  Google Scholar 

  • Rabaey K, Boon N, Siciliano SD, Verhaege M, Verstraete W (2004) Biofuel cells select for microbial consortia that self-mediate electron transfer. Appl Environ Microbiol 70:5373–5382

    Article  CAS  Google Scholar 

  • Rismani-Yazdi H, Christy AD, Dehority BA, Morrison M, Yu Z, Tuovinen OH (2007) Electricity generation from cellulose by rumen microorganisms in microbial fuel cells. Biotechnol Bioeng 97:1398–1407

    Article  CAS  Google Scholar 

  • Rittmann BE, Krajmalnik-Brown R, Halden RU (2008) Pre-genomic, genomic and post-genomic study of microbial communities involved in bioenergy. Nat Rev Micro 6:604–612

    Article  CAS  Google Scholar 

  • Röling WFM, van Breukelen BM, Braster M, Goeltom MT, Groen J, van Verseveld HW (2000) Analysis of microbial communities in a landfill leachate polluted aquifer using a new method for anaerobic physiological profiling and 16S rDNA based fingerprinting. Microb Ecol 40:177–188

    Google Scholar 

  • SFS 5504 (1988) Determination of chemical oxygen demand (CODCr) in water with the closed tube method oxidation of dichromate. Finnish Standards Association SFS, Helsinki

    Google Scholar 

  • Smith NR, Yu Z, Mohn WW (2003) Stability of the bacterial community in a pulp mill effluent treatment system during normal operation and a system shutdown. Water Res 37:4873–4884

    Article  CAS  Google Scholar 

  • Smith RL, Buckwalter SP, Repert DA, Miller DN (2005) Small-scale, hydrogen-oxidizing-denitrifying bioreactor for treatment of nitrate-contaminated drinking water. Water Res 39:2014–2023

    Article  CAS  Google Scholar 

  • Urich T, Lanzén A, Qi J, Huson DH, Schleper C, Schuster SC (2008) Simultaneous assessment of soil microbial community structure and function through analysis of the meta-transcriptome. PloS ONE 3:1–13

    Article  Google Scholar 

  • Van Versevelde HW, Röling WFM (2004) Cluster analysis and statistical comparison of molecular community profile data. In: Kowalchuk GA, De Bruijn FJ, Head IM, Akkermans AD (eds) Molecular microbial ecology manual. Kluwer Academic, Dordrecht, pp 1373–1396

    Google Scholar 

  • Vandamme P, Vancanneyt M, Pot B, Mels L, Hoste B, Dewettinck D, Vlaes L, van den Borre C, Higgins R, Hommez J, Kersters K, Butzler J-P, Goossens H (1992) Polyphasic taxonomic study of the emended genus Arcobacter with Arcobacter butzleri comb. nov. and Arcobacter skirrowii sp. nov., an aerotolerant bacterium isolated from veterinary specimens. Int J Syst Bacteriol 42:344–356

    Article  CAS  Google Scholar 

  • Wang X, Feng Y, Wang H, Qu Y, Yu Y, Ren N, Li N, Wang E, Lee H, Logan BE (2009) Bioaugmentation for electricity generation from corn stover biomass using microbial fuel cells. Environ Sci Technol 43:6088–6093

    Article  CAS  Google Scholar 

  • Wauters G, De Baere T, Willems A, Falsen E, Vaneechouette M (2003) Description of Comamonas aquatica comb. nov. and Comamonas kerstersii sp. nov. for two subgroups of Comamonas terrigena and emended description of Comamonas terrigena. Int J Syst Evol Microbiol 53:859–862

    Article  CAS  Google Scholar 

  • White HK, Reimers CE, Cordes EE, Dilly GF, Girguis PR (2009) Quantitative population dynamics of microbial communities in plankton-fed microbial fuel cells. ISME J 3:635–646

    Article  Google Scholar 

  • Wittebolle L, Marzorati M, Clement L, Balloi A, Daffonchio D, Heylen K, De Vos P, Verstraete W, Boon N (2009a) Initial community evenness favours functionality under selective stress. Nature 458:623–626

    Article  CAS  Google Scholar 

  • Wittebolle L, Van Vooren N, Verstraete W, Boon N (2009b) High reproducibility of ammonia-oxidizing bacterial communities in parallel sequential batch reactors. J Appl Microbiol 107:385–394

    Article  CAS  Google Scholar 

  • Wrighton KC, Agbo P, Warnecke F, Weber KA, Brodie EL, DeSantis TZ, Hugenholtz P, Andersen GL, Coates JD (2008) A novel ecological role of the Firmicutes identified in thermophilic microbial fuel cells. ISME J 2:1146–1156

    Article  CAS  Google Scholar 

  • Wrighton KC, Virdis B, Clauwaert P, Read ST, Daly RA, Boon N, Piceno Y, Andersen GL, Coates JD, Rabaey K (2010) Bacterial community structure corresponds to performance during cathodic nitrate reduction. ISME J 4:1443–1455

    Article  CAS  Google Scholar 

  • Xing D, Zuo Y, Cheng S, Regan JM, Logan BE (2008) Electricity generation by Rhodopseudomonas palustris DX-1. Environ Sci Technol 42:4146–4151

    Article  CAS  Google Scholar 

  • Xing D, Cheng S, Regan JM, Logan BE (2009) Change in microbial communities in acetate- and glucose-fed microbial fuel cells in the presence of light. Biosens Bioelectron 49:105–111

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Yi H, Nevin KP, Kim BH, Franks AE, Klimes A, Tender LM, Lovley DR (2009) Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens Bioelectron 24:3498–3503

    Article  CAS  Google Scholar 

  • Zhang T, Fang HHP (2000) Digitization of DGGE (denaturing gradient gel electrophoresis) profile and cluster analysis of microbial communities. Biotechnol Lett 22:399–405

    Article  CAS  Google Scholar 

  • Zhang Y, Min B, Huang L, Angelidaki I (2009) Generation of electricity and analysis of microbial communities in wheat straw biomass-powered microbial fuel cells. Appl Environ Microbiol 75:3389–3395

    Article  CAS  Google Scholar 

  • Zhao F, Rahunen N, Varcoe JR, Chandra A, Avignone-Rossa C, Thumser AE, Slade RCT (2008) Activated carbon cloth as anode for sulfate removal in a microbial fuel cell. Environ Sci Technol 42:4971–4976

    Article  CAS  Google Scholar 

  • Zuo Y, Xing D, Regan JM, Logan BE (2008) Isolation of the exoelectrogenic bacterium Ochrobactrum anthropi YZ-1 by using a U-tube microbial fuel cell. Appl Environ Microbiol 74:3130–3137

    Article  CAS  Google Scholar 

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Acknowledgements

This research was funded by the Research Councils UK Energy Programme as the Supergen 5 Biological Fuel Cells Consortium (managed by the Engineering and Physical Sciences Research Council: Grants EP/D047943/1 and EP/H019480/1).

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  1. Feng Zhao

    Present address: Institute of Urban Environment, CAS, Xiamen, 361021, China

Authors and Affiliations

  1. Division of Microbial Sciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford, GU2 7XH, UK

    Nelli J. Beecroft & Claudio Avignone-Rossa

  2. Division of Biochemical Sciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford, GU2 7XH, UK

    Alfred E. Thumser

  3. Division of Chemical Sciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford, GU2 7XH, UK

    Feng Zhao, John R. Varcoe & Robert C. T. Slade

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  1. Nelli J. Beecroft
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Beecroft, N.J., Zhao, F., Varcoe, J.R. et al. Dynamic changes in the microbial community composition in microbial fuel cells fed with sucrose. Appl Microbiol Biotechnol 93, 423–437 (2012). https://doi.org/10.1007/s00253-011-3590-y

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