Applied Microbiology and Biotechnology

, Volume 97, Issue 3, pp 1299–1315 | Cite as

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

  • Stefano Mocali
  • Carlo Galeffi
  • Elena Perrin
  • Alessandro Florio
  • Melania Migliore
  • Francesco Canganella
  • Giovanna Bianconi
  • Elena Di Mattia
  • Maria Teresa Dell’Abate
  • Renato Fani
  • Anna Benedetti
Environmental biotechnology

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.

Keywords

Microbial fuel cells Soil Organic matter Electrogenic bacteria Microbial diversity Humification 

Notes

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).

Supplementary material

253_2012_3906_MOESM1_ESM.ppt (140 kb)
Additional file 1 Phylogenetic trees (all samples) (PPT 140 kb)

References

  1. 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 40:3388–3394CrossRefGoogle Scholar
  2. 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 25:3389–3402CrossRefGoogle Scholar
  3. Bond DR, Lovley DR (2003) Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555CrossRefGoogle Scholar
  4. Bond DR, Holmes DE, Tender LM, Lovley DR (2002) Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485CrossRefGoogle Scholar
  5. Brüchert V, Arnosti C (2003) Anaerobic carbon transformation: experimental studies with flow-through cells. Mar Chem 80:171–183CrossRefGoogle Scholar
  6. 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):1481–1484Google Scholar
  7. Ciavatta C, Govi M, Vittori Antisari L, Sequi P (1990) Characterization of humified compounds by extraction and fractionation on solid polyvinylpyrrolidone. J Chromatogr 509:141–146CrossRefGoogle Scholar
  8. 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):1504–1509Google Scholar
  9. 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):2445–2452CrossRefGoogle Scholar
  10. 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–D145CrossRefGoogle Scholar
  11. 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 42:3053–3058CrossRefGoogle Scholar
  12. Dell’Abate MT, Benedetti A, Sequi P (2000) Thermal methods of organic matter maturation monitoring during a composting process. J Therm Anal Calorim 61:389–396CrossRefGoogle Scholar
  13. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113CrossRefGoogle Scholar
  14. 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 64:871–879Google Scholar
  15. 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 119–126Google Scholar
  16. 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 127:85–91CrossRefGoogle Scholar
  17. 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 48:178–190CrossRefGoogle Scholar
  18. Hong SW, Kim HS, Chung TH (2010) Alteration of sediment organic matter in sediment microbial fuel cells. Environ Pollut 158:185–191CrossRefGoogle Scholar
  19. 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 8:6CrossRefGoogle Scholar
  20. Jiang J, Zhao Q, Wei L, Wang K (2010) Extracellular biological organic matters in microbial fuel cell using sewage sludge as fuel. Water Res 44:2163–2170CrossRefGoogle Scholar
  21. 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 63:672–681CrossRefGoogle Scholar
  22. 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 101:698–710CrossRefGoogle Scholar
  23. Kim BH, Chang IS, Gadd GM (2007a) Challenges in microbial fuel cell development and operation. Appl Microbiol Biotechnol 76:485–494CrossRefGoogle Scholar
  24. Kim JR, Jung S, Regan JM, Logan BE (2007b) Electricity generation and microbial community analysis of alcohol powered microbial fuel cells. Bioresour Technol 98:2568–2577CrossRefGoogle Scholar
  25. Kimura MA (1980) Simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:11–120CrossRefGoogle Scholar
  26. 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 26:173–187CrossRefGoogle Scholar
  27. 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 223:185–191CrossRefGoogle Scholar
  28. Leinweber P, Schulten HR (1999) Advances in analytical pyrolysis of soil organic matter. J Anal Appl Pyrol 49:359–383CrossRefGoogle Scholar
  29. Liu H, Ramnarayanan R, Logan B (2004) Production of electricity during wastewater treatment using a single chamber microbial fuel cell. Environ Sci Technol 38:2281–2285CrossRefGoogle Scholar
  30. 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 96:358–371CrossRefGoogle Scholar
  31. Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381CrossRefGoogle Scholar
  32. Logan BE (2010) Scaling up microbial fuel cells and other bioelectrochemical systems. Appl Microbiol Biotechnol 85:1665–1671CrossRefGoogle Scholar
  33. Logan BE, Regan JM (2006a) Microbial fuel cells—challenges and applications. Environ Sci Technol 1:5172–5180CrossRefGoogle Scholar
  34. Logan BE, Regan JM (2006b) Electricity-producing bacterial communities in microbial fuel cells. Trends Microbiol 14(12):512–518CrossRefGoogle Scholar
  35. Logan BE, Murano C, Scott K, Gray ND, Head IM (2005) Electricity generation from cysteine in a microbial fuel cell. Water Res 39:942–952CrossRefGoogle Scholar
  36. 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 68:136–140Google Scholar
  37. Lovley DR (2008) The microbe electric: conversion of organic matter to electricity. Curr Opin Biotechnol 19:1–8CrossRefGoogle Scholar
  38. Mathis BJ, Marshall CW, Milliken CE, Makkar RS, Creager SE, May HD (2008) Electricity generation by thermophilic microorganisms from marine sediment. Appl Microbiol Biotechnol 78:147–155CrossRefGoogle Scholar
  39. Min B, Kim J, Oha S, Regana JM, Logan BE (2005) Electricity generation from swine wastewater using microbial fuel cells. Water Res 39:4961–4968CrossRefGoogle Scholar
  40. 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 150:83–93CrossRefGoogle Scholar
  41. Morris JM, Jin S, Crimi B, Pruden A (2009) Microbial fuel cell in enhancing anaerobic biodegradation of diesel. Chem Eng J 146:161–167CrossRefGoogle Scholar
  42. Niessen J, Schroder U, Scholz F (2004) Exploiting complex carbohydrates for microbial electricity generation—a bacterial fuel cell operating on starch. Electrochem Commun 6:955–958CrossRefGoogle Scholar
  43. 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 8:869–873CrossRefGoogle Scholar
  44. 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 101:1533–1543CrossRefGoogle Scholar
  45. 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 233:77–82CrossRefGoogle Scholar
  46. Rabaey K, Boon N, Höfte M, Verstraete W (2005) Microbial phenazine production enhances electron transfer in biofuel cells. Environ Sci Technol 39:3401–3408CrossRefGoogle Scholar
  47. 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 1:9–18CrossRefGoogle Scholar
  48. Rabeay K, Vestraete W (2005) Microbial fuel cells: novel biotechnology for energy generation. Trends Biotechnol 23(6):291–298CrossRefGoogle Scholar
  49. 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):5373–5382CrossRefGoogle Scholar
  50. Reimers CE, Tender LM, Fertig S, Wang W (2001) Harvesting energy from the marine sediment–water interface. Environ Sci Technol 35:192–195CrossRefGoogle Scholar
  51. 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):7029–7040CrossRefGoogle Scholar
  52. 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 97:1398–1407CrossRefGoogle Scholar
  53. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  54. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467Google Scholar
  55. Scott K, Murano C (2007) A study of a microbial fuel cell battery using manure sludge waste. J Chem Technol Biotechnol 82:809–817CrossRefGoogle Scholar
  56. Sleator RD, Shortall C, Hill C (2008) Metagenomics. Lett Appl Microbiol 47:361–366CrossRefGoogle Scholar
  57. 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 64:1CrossRefGoogle Scholar
  58. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefGoogle Scholar
  59. 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 20:821–825Google Scholar
  60. Virkutyte J, Sillanpää M, Latostenmaa P (2002) Electrokinetic soil remediation—critical overview. Sci Total Environ 289(1–3):97–121CrossRefGoogle Scholar
  61. 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 18:6531–6535CrossRefGoogle Scholar
  62. 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):3389–3395CrossRefGoogle Scholar
  63. Zuo Y, Maness PC, Logan BE (2006) Electricity production from steam-exploded corn stover biomass. Energy Fuel 20:1716–1721CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Stefano Mocali
    • 1
    • 2
  • Carlo Galeffi
    • 2
  • Elena Perrin
    • 3
  • Alessandro Florio
    • 2
  • Melania Migliore
    • 2
  • Francesco Canganella
    • 4
  • Giovanna Bianconi
    • 4
  • Elena Di Mattia
    • 5
  • Maria Teresa Dell’Abate
    • 2
  • Renato Fani
    • 3
  • Anna Benedetti
    • 2
  1. 1.CRA—Agrobiology and Pedology Research CentreFirenzeItaly
  2. 2.CRA—Research Centre for the Soil–Plant SystemRomaItaly
  3. 3.Evolutionary Biology DepartmentUniversity of FlorenceFirenzeItaly
  4. 4.Department for Innovation in Biological, Agrofood and Forest systemsUniversity of TusciaViterboItaly
  5. 5.Department of Sciences and Technologies for Agriculture, Forest, Nature and EnergyUniversity of TusciaViterboItaly

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