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Alteration of bacterial communities and organic matter in microbial fuel cells (MFCs) supplied with soil and organic fertilizer

  • Environmental biotechnology
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Abstract

The alteration of the organic matter (OM) and the composition of bacterial community in microbial fuel cells (MFCs) supplied with soil (S) and a composted organic fertilizer (A) was examined at the beginning and at the end of 3 weeks of incubation under current-producing as well as no-current-producing conditions. Denaturing gradient gel electrophoresis revealed a significant alteration of the microbial community structure in MFCs generating electricity as compared with no-current-producing MFCs. The genetic diversity of cultivable bacterial communities was assessed by random amplified polymorphic DNA (RAPD) analysis of 106 bacterial isolates obtained by using both generic and elective media. Sequencing of the 16S rRNA genes of the more representative RAPD groups indicated that over 50.4% of the isolates from MFCs fed with S were Proteobacteria, 25.1% Firmicutes, and 24.5% Actinobacteria, whereas in MFCs supplied with A 100% of the dominant species belonged to γ-Proteobacteria. The chemical analysis performed by fractioning the OM and using thermal analysis showed that the amount of total organic carbon contained in the soluble phase of the electrochemically active chambers significantly decreased as compared to the no-current-producing systems, whereas the OM of the solid phase became more humified and aromatic along with electricity generation, suggesting a significant stimulation of a humification process of the OM. These findings demonstrated that electroactive bacteria are commonly present in aerobic organic substrates such as soil or a fertilizer and that MFCs could represent a powerful tool for exploring the mineralization and humification processes of the soil OM.

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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 Tech 40:3388–3394

    Article  CAS  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res 25:3389–3402

    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 

  • Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485

    Article  CAS  Google Scholar 

  • Brüchert V, Arnosti C (2003) Anaerobic carbon transformation: experimental studies with flow-through cells. Mar Chem 80:171–183

    Article  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(9):1481–1484

    CAS  Google Scholar 

  • Ciavatta C, Govi M, Vittori Antisari L, Sequi P (1990) Characterization of humified compounds by extraction and fractionation on solid polyvinylpyrrolidone. J Chromatogr 509:141–146

    Article  CAS  Google Scholar 

  • Coates JD, Ellis DJ, Blunt-Harris EL, Gaw CV, Roden EE, Lovley DR (1998) Recovery of humic-reducing bacteria from a diversity of environments. Appl Environ Microbiol 64(4):1504–1509

    CAS  Google Scholar 

  • Coates JD, Cole KA, Chakraborty R, O’Connor SM, Achenbach LA (2002) Diversity and ubiquity of bacteria capable of utilizing humic substances as electron donors for anaerobic respiration. Appl Environ Microbiol 68(5):2445–2452

    Article  CAS  Google Scholar 

  • Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, Kulam-Syed-Mohideen AS, McGarrell DM, Marsh T, Garrity GM, Tiedje J (2009) The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145

    Article  CAS  Google Scholar 

  • De Schamphelaire L, van Den Bossche V, Dang HS, Höfte M, Boon N, Rabaey K, Verstraete W (2008) Microbial fuel cells generating electricity from rhizodeposits of rice plants. Environ Sci Technol 42:3053–3058

    Article  Google Scholar 

  • Dell’Abate MT, Benedetti A, Sequi P (2000) Thermal methods of organic matter maturation monitoring during a composting process. J Therm Anal Calorim 61:389–396

    Article  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113

    Article  Google Scholar 

  • Felske A, Wolterink A, Van Lis R, Akkermans ADL (1998) Phylogeny of the main bacterial 16S rRNA sequences in Drentse A grassland soils (The Netherlands). Appl Environ Microbiol 64:871–879

    CAS  Google Scholar 

  • Flaig W, Beutelspacher H, Rietz E (1975) Chemical composition and physical properties of humic substances. In: Gieseking JE (ed) Soil components, vol. 1. Springer, Berlin, pp 119–126

    Google Scholar 

  • Grifoni A, Bazzicalupo M, Di Serio C, Fancelli S, Fani R (1995) Identification of Azospirillum strains by restriction fragment length polymorphism of the 16S rDNA and of the histidine operon. FEMS Microbiol Lett 127:85–91

    Article  CAS  Google Scholar 

  • Holmes DE, Bond DR, O’Neill RA, Reimers CE, Tender LR, Lovley DR (2004) Microbial communities associated with electrodes harvesting electricity from a variety of aquatic sediments. Microb Ecol 48:178–190

    Article  CAS  Google Scholar 

  • Hong SW, Kim HS, Chung TH (2010) Alteration of sediment organic matter in sediment microbial fuel cells. Environ Pollut 158:185–191

    Article  CAS  Google Scholar 

  • Ishii S, Shimoyama T, Hotta Y, Watanabe K (2008) Characterization of a filamentous biofilm community established in a cellulose-fed microbial fuel cell. BMC Microbiol 8:6

    Article  Google Scholar 

  • Jiang J, Zhao Q, Wei L, Wang K (2010) Extracellular biological organic matters in microbial fuel cell using sewage sludge as fuel. Water Res 44:2163–2170

    Article  CAS  Google Scholar 

  • Kim BH, Park HS, Kim HJ, Kim GT, Chang IS, Lee J, Phung NT (2004) Enrichment of microbial community generating electricity using a fuel-cell-type electrochemical cell. Appl Microbiol Biotechnol 63:672–681

    Article  CAS  Google Scholar 

  • Kim GT, Webster G, Wimpenny JWT, Kim BH, Kim HJ, Weightman AJ (2006) Bacterial community structure, compartmentalization and activity in microbial fuel cells. J Appl Microbiol 101:698–710

    Article  CAS  Google Scholar 

  • Kim BH, Chang IS, Gadd GM (2007a) Challenges in microbial fuel cell development and operation. Appl Microbiol Biotechnol 76:485–494

    Article  CAS  Google Scholar 

  • Kim JR, Jung S, Regan JM, Logan BE (2007b) Electricity generation and microbial community analysis of alcohol powered microbial fuel cells. Bioresour Technol 98:2568–2577

    Article  CAS  Google Scholar 

  • Kimura MA (1980) Simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:11–120

    Article  Google Scholar 

  • Klammer S, Knapp B, Insam H, Dell’Abate MT, Ros M (2008) Bacterial community patterns and thermal analyses of composts of various origins. Waste Manag Res 26:173–187

    Article  Google Scholar 

  • Lee J, Phung NT, Chang IS, Kim BH, Sung HC (2003) Use of acetate for enrichment of electrochemically active microorganisms and their 16S rDNA analyses. FEMS Microbiol Lett 223:185–191

    Article  CAS  Google Scholar 

  • Leinweber P, Schulten HR (1999) Advances in analytical pyrolysis of soil organic matter. J Anal Appl Pyrol 49:359–383

    Article  CAS  Google Scholar 

  • Liu H, Ramnarayanan R, Logan B (2004) Production of electricity during wastewater treatment using a single chamber microbial fuel cell. Environ Sci Technol 38:2281–2285

    Article  CAS  Google Scholar 

  • Lluch AV, Felipe AM, Greus AR, Cadenato A, Ramis X, Salla JM, Morancho JM (2005) Thermal analysis characterization of the degradation of biodegradable starch blends in soil. J Appl Polym Sci 96:358–371

    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 (2010) Scaling up microbial fuel cells and other bioelectrochemical systems. Appl Microbiol Biotechnol 85:1665–1671

    Article  CAS  Google Scholar 

  • Logan BE, Regan JM (2006a) Microbial fuel cells—challenges and applications. Environ Sci Technol 1:5172–5180

    Article  Google Scholar 

  • Logan BE, Regan JM (2006b) Electricity-producing bacterial communities in microbial fuel cells. Trends Microbiol 14(12):512–518

    Article  CAS  Google Scholar 

  • Logan BE, Murano C, Scott K, Gray ND, Head IM (2005) Electricity generation from cysteine in a microbial fuel cell. Water Res 39:942–952

    Article  CAS  Google Scholar 

  • Lopez-Capel E, Sohi SP, Gaunt JL, Manning DAC (2005) Use of thermogravimetry-differential scanning calorimetry to characterize modelable soil organic matter fractions. Soil Sci Soc Am J 68:136–140

    Google Scholar 

  • Lovley DR (2008) The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 19:1–8

    Article  Google Scholar 

  • Mathis BJ, Marshall CW, Milliken CE, Makkar RS, Creager SE, May HD (2008) Electricity generation by thermophilic microorganisms from marine sediment. Appl Microbiol Biotechnol 78:147–155

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mori E, Lio’ P, Daly S, Damiani G, Perito B, Fani R (1999) Molecular nature of RAPD markers amplified from Haemophilus influenzae Rd genome. Res Microbiol 150:83–93

    Article  CAS  Google Scholar 

  • Morris JM, Jin S, Crimi B, Pruden A (2009) Microbial fuel cell in enhancing anaerobic biodegradation of diesel. Chem Eng J 146:161–167

    Article  CAS  Google Scholar 

  • Niessen J, Schroder U, Scholz F (2004) Exploiting complex carbohydrates for microbial electricity generation—a bacterial fuel cell operating on starch. Electrochem Commun 6:955–958

    Article  CAS  Google Scholar 

  • Niessen J, Harnisch F, Rosenbaum M, Schroder U, Scholz F (2006) Heat treated soil as convenient and versatile source of bacterial communities for microbial electricity generation. Electrochem Commun 8:869–873

    Article  CAS  Google Scholar 

  • Pant D, Van Bogaert G, Diels L, Vanbroekhoven K (2010) A review of the substrates used in microbial fuel cells (MFCs) for sustainable energy production. Bioresource Technol 101:1533–1543

    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, Boon N, Höfte M, Verstraete W (2005) Microbial phenazine production enhances electron transfer in biofuel cells. Environ Sci Technol 39:3401–3408

    Article  CAS  Google Scholar 

  • Rabaey K, Rodríguez J, Blackall LL, Keller J, Gross P, Batstone D, Verstraete W, Nealson KH (2007) Microbial ecology meets electrochemistry: electricity-driven and driving communities. ISME J 1:9–18

    Article  CAS  Google Scholar 

  • Rabeay K, Vestraete W (2005) Microbial fuel cells: novel biotechnology for energy generation. Trends Biotechnol 23(6):291–298

    Article  Google Scholar 

  • Rabeay 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(9):5373–5382

    Article  Google Scholar 

  • Reimers CE, Tender LM, Fertig S, Wang W (2001) Harvesting energy from the marine sediment–water interface. Environ Sci Technol 35:192–195

    Article  CAS  Google Scholar 

  • Reimers CE, Stecher HA III, Westall JC, Alleau Y, Howell KA, Soule L, White HK, Girguis PR (2007) Substrate degradation kinetics, microbial diversity and current efficiency of microbial fuel cells supplied with marine plankton. Appl Environ Microbiol 73(21):7029–7040

    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 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • Scott K, Murano C (2007) A study of a microbial fuel cell battery using manure sludge waste. J Chem Technol Biotechnol 82:809–817

    Article  CAS  Google Scholar 

  • Sleator RD, Shortall C, Hill C (2008) Metagenomics. Lett Appl Microbiol 47:361–366

    Article  CAS  Google Scholar 

  • Springer U, Klee J (1954) Prüfung der Leistungsfähigkeit von einigen wichtigeren Verfahren zur Bestimmung des Kohlemstoffs mittels Chromschwefelsäure sowie Vorschlag einer neuen Schnellmethode. Z Pflanzenernähr Dang Bodenk 64:1

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  Google Scholar 

  • Tender LM, Reimers CE, Stecher HA III, Holmes DE, Bond DR, Lowy DA, Pilobello K, Fertig SJ, Lovley DR (2002) Harnessing microbially generated power on the seafloor. Nat Biotechnol 20:821–825

    CAS  Google Scholar 

  • Virkutyte J, Sillanpää M, Latostenmaa P (2002) Electrokinetic soil remediation—critical overview. Sci Total Environ 289(1–3):97–121

    Article  CAS  Google Scholar 

  • Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acid Res 18:6531–6535

    Article  CAS  Google Scholar 

  • Zhang Y, Min B, Huang L, Angelidaki I (2009) Generation of electricity and analysis of microbial communities in wheat straw biomasses-powered microbial fuel cells. Appl Environ Microbiol 75(11):3389–3395

    Article  CAS  Google Scholar 

  • Zuo Y, Maness PC, Logan BE (2006) Electricity production from steam-exploded corn stover biomass. Energy Fuel 20:1716–1721

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported with funds from the Italian Ministry of Agricultural, Food, and Forestry Policies (MIPAAF) and it is part of the results of the BEM project (D.M. 247/07).

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Correspondence to Stefano Mocali.

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Phylogenetic trees (all samples) (PPT 140 kb)

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Mocali, S., Galeffi, C., Perrin, E. et al. Alteration of bacterial communities and organic matter in microbial fuel cells (MFCs) supplied with soil and organic fertilizer. Appl Microbiol Biotechnol 97, 1299–1315 (2013). https://doi.org/10.1007/s00253-012-3906-6

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  • DOI: https://doi.org/10.1007/s00253-012-3906-6

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