Microbial community structure elucidates performance of Glyceria maxima plant microbial fuel cell
Abstract
The plant microbial fuel cell (PMFC) is a technology in which living plant roots provide electron donor, via rhizodeposition, to a mixed microbial community to generate electricity in a microbial fuel cell. Analysis and localisation of the microbial community is necessary for gaining insight into the competition for electron donor in a PMFC. This paper characterises the anode–rhizosphere bacterial community of a Glyceria maxima (reed mannagrass) PMFC. Electrochemically active bacteria (EAB) were located on the root surfaces, but they were more abundant colonising the graphite granular electrode. Anaerobic cellulolytic bacteria dominated the area where most of the EAB were found, indicating that the current was probably generated via the hydrolysis of cellulose. Due to the presence of oxygen and nitrate, short-chain fatty acid-utilising denitrifiers were the major competitors for the electron donor. Acetate-utilising methanogens played a minor role in the competition for electron donor, probably due to the availability of graphite granules as electron acceptors.
Related Content
Supplementary Material (0)
References (62)
- Amann RI, Krumholz L, Stahl DA (1990) Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172:762–770
- Amann RI, Zarda B, Stahl DA, Schleifer KH (1992) Identification of individual prokaryotic cells by using enzyme-labeled, rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 58:3007–3011
- Bano N, Ruffin S, Ransom B, Hollibaugh JT (2004) Phylogenetic composition of arctic ocean archaeal assemblages and comparison with Antarctic assemblages. Appl Environ Microbiol 70:781–789 CrossRef
- Bond DR, Lovley DR (2002) Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environ Microbiol 4:115–124 CrossRef
- Borole AP, Hamilton CY, Aaron DS, Tsouris C (2009) Investigating microbial fuel cell bioanode performance under different cathode conditions. Biotechnol Progr 25:1630–1636
- Chaudhuri SK, Lovley DR (2003) Electricity generation by direct oxidation of glucose in mediatorless microbial fuel cells. Nat Biotechnol 21:1229–1232 CrossRef
- Coates JD, Bhupathiraju VK, Achenbach LA, McInerney MJ, Lovley DR (2001) Geobacter hydrogenophilus, Geobacter chapellei and Geobacter grbiciae, three new, strictly anaerobic, dissimilatory Fe(III)-reducers. Int J Syst Evol Microbiol 51:581–588
- Collins MD, Lawson PA, Willems A, Cordoba JJ, Fernandez-Garayzabal J, Garcia P, Cai J, Hippe H, Farrow JAE (1994) The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int J Syst Bacteriol 44:812–826 CrossRef
- Daims H, Brähl A, Amann R, Schleifer KH, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444 CrossRef
- De Schamphelaire L, Van Den Bossche L, Hai SD, Hofte M, Boon N, Rabaey K, Verstraete W (2008) Microbial fuel cells generating electricity from rhizodeposits of rice plants. Environ Sci Technol 42:3053–3058 CrossRef
- De Schamphelaire L, Cabezas A, Marzorati M, Friedrich MW, Boon N, Verstraete W (2010) Microbial community analysis of anodes from sediment microbial fuel cells powered by rhizodeposits of living rice plants. Appl Environ Microbiol 76:2002–2008 CrossRef
- Dekker A, Ter Heijne A, Saakes M, Hamelers HVM, Buisman CJN (2009) Analysis and improvement of a scaled-up and stacked microbial fuel cell. Environ Sci Technol 43:9038–9042 CrossRef
- Demaneche S, Sanguin H, Poté J, Navarro E, Bernillon D, Mavingui P, Wildi W, Vogel TM, Simonet P (2008) Antibiotic-resistant soil bacteria in transgenic plant fields. Proc Natl Acad Sci USA 105:3957–3962 CrossRef
- Finneran KT, Johnsen CV, Lovley DR (2003) Rhodoferax ferrireducens sp. nov., a psychrotolerant, facultatively anaerobic bacterium that oxidizes acetate with the reduction of Fe(III). Int J Syst Evol Microbiol 53:669–673 CrossRef
- Franks AH, Harmsen HJM, Raangs GC, Jansen GJ, Schut F, Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64:3336–3345
- Ginige MP, Keller J, Blackall LL (2005) Investigation of an acetate-fed denitrifying microbial community by stable isotope probing, full-cycle rRNA analysis, and fluorescent in situ hybridization-microautoradiography. Appl Environ Microbiol 71:8683–8691 CrossRef
- Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2000) Rapid method for coextraction of DNA and RNA from natural environments for analysis of ribosomal DNA- and rRNA-based microbial community composition. Appl Environ Microbiol 66:5488–5491 CrossRef
- Harmsen HJM, Raangs GC, He T, Degener JE, Welling GW (2002) Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol 68:2982–2990 CrossRef
- Hartmann A, Schmid M, van Tuinen D, Berg G (2009) Plant-driven selection of microbes. Plant Soil 321:235–257 CrossRef
- Helder M, Strik DPBTB, Hamelers HVM, Kuhn AJ, Blok C, Buisman CJN (2010) Concurrent bio-electricity and biomass production in three plant–microbial fuel cells using Spartina anglica, Arundinella anomala and Arundo donax. Bioresource Technol 101:3541–3547 CrossRef
- Holmes DE, Bond DR, O’Neil 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 CrossRef
- Hsiao CL, Chang JJ, Wu JH, Chin WC, Wen FS, Huang CC, Chen CC, Lin CY (2009) Clostridium strain co-cultures for biohydrogen production enhancement from condensed molasses fermentation solubles. Int J Hydrogen Energy 34:7173–7181 CrossRef
- Ishii S, Hotta Y, Watanabe K (2008) Methanogenesis versus electrogenesis: morphological and phylogenetic comparisons of microbial communities. Biosci Biotechnol Biochem 72:286–294 CrossRef
- 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 CrossRef
- Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Röser A, Koops HP, Wagner M (1998) Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge: Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol 64:3042–3051
- Kaku N, Yonezawa N, Kodama Y, Watanabe K (2008) Plant/microbe cooperation for electricity generation in a rice paddy field. Appl Microbiol Biotechnol 79:43–49 CrossRef
- Kim BH, Kim HJ, Hyun MS, Park DH (1999) Direct electrode reaction of Fe(III)-reducing bacterium, Shewanella putrefaciens. J Microbiol Biotechnol 9:127–131
- Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrand E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics, 1st edn. Wiley, New York, pp 115–175
- Lovley DR, Kashefi K, Vargas M, Tor JM, Blunt-Harris EL (2000) Reduction of humic substances and Fe(III) by hyperthermophilic microorganisms. Chem Geol 169:289–298 CrossRef
- Lynd LR, Wyman CE, Gerngross TU (1999) Biocommodity engineering. Biotechnol Progr 15:777–793 CrossRef
- Lynd LR, Weimer PJ, Van Zyl WH, Pretorius IS (2002) Microbial cellulose utilization: fundamentals and biotechnology. Microbiol Mol Biol Rev 66:506–577 CrossRef
- Maki M, Leung KT, Qin W (2009) The prospects of cellulase-producing bacteria for the bioconversion of lignocellulosic biomass. Int J Biol Sci 5:500–516 CrossRef
- Manz W, Amann R, Ludwig W, Wagner M, Schleifer K-H (1992) Phylogenetic oligodeoxynucleotide probes for the major subclass of proteobacteria: problems and solutions. Syst Appl Microbiol 15:593–600 CrossRef
- Min B, Cheng S, Logan BE (2005) Electricity generation using membrane and salt bridge microbial fuel cells. Water Res 39:1675–1686 CrossRef
- Nicol GW, Glover LA, Prosser JI (2003) Molecular analysis of methanogenic archaeal communities in managed and natural upland pasture soils. Global Change Biol 9:1451–1457 CrossRef
- Nielsen JL, Klausen C, Nielsen PH, Burford M, Jørgensen NOG (2006) Detection of activity among uncultured actinobacteria in a drinking water reservoir. FEMS Microbiol Ecol 55:432–438 CrossRef
- Niessen J, Schröder U, Scholz F (2004) Exploiting complex carbohydrates for microbial electricity generation—a bacterial fuel cell operating on starch. Electrochem Commun 6:955–958 CrossRef
- Offre P, Pivato B, Siblot S, Gamalero E, Corberand T, Lemanceau P, Mougel C (2007) Identification of bacterial groups preferentially associated with mycorrhizal roots of Medicago truncatula. Appl Environ Microbiol 73:913–921 CrossRef
- Park DH, Kim BH (2001) Growth properties of the iron-reducing bacteria, Shewanella putrefaciens IR-1 and MR-1 coupling to reduction of Fe(III) to Fe(II). J Microbiol 39:273–278
- Park HS, Kim BH, Kim HS, Kim HJ, Kim GT, Kim M, Chang IS, Park YK, Chang HI (2001) A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Clostridium butyricum isolated from a microbial fuel cell. Anaerobe 7:297–306 CrossRef
- Phillips DA, Ferris H, Cook DR, Strong DR (2003) Molecular control points in rhizosphere food webs. Ecology 84:816–826 CrossRef
- Pinton R, Varanini Z (2007) The rhizosphere: biochemistry and organic substances at the soil–plant interface. CRC, Boca Raton CrossRef
- Potter MC (1911) Electrical effects accompanying the decomposition of organic compounds. Proc R Soc London, Ser B 84:260–276 CrossRef
- 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 CrossRef
- Reguera G, Nevin KP, Nicoll JS, Covalla SF, Woodard TL, Lovley DR (2006) Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 72:7345–7348 CrossRef
- Ren Z, Ward TE, Regan JM (2007) Electricity production from cellulose in a microbial fuel cell using a defined binary culture. Environ Sci Technol 41:4781–4786 CrossRef
- Rezaei F, Xing D, Wagner R, Regan JM, Richard TL, Logan BE (2009) Simultaneous cellulose degradation and electricity production by Enterobacter cloacae in a microbial fuel cell. Appl Environ Microbiol 75:3673–3678 CrossRef
- 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 CrossRef
- Scheid D, Stubner S, Conrad R (2004) Identification of rice root associated nitrate, sulfate and ferric iron reducing bacteria during root decomposition. FEMS Microbiol Ecol 50:101–110 CrossRef
- Schellenberger S, Kolb S, Drake HL (2010) Metabolic responses of novel cellulolytic and saccharolytic agricultural soil bacteria to oxygen. Environ Microbiol 12:845–861 CrossRef
- Strik DPBTB, Hamelers HVM, Snel JFH, Buisman CJN (2008) Green electricity production with living plants and bacteria in a fuel cell. Int J Energy Res 32:870–876 CrossRef
- Strik DPBTB, Timmers RA, Helder M, Steinbusch KJJ, Hamelers HVM, Buisman CJN (2011) Microbial solar cells: applying photosynthetic and electrochemically active organisms. Trends Biotechnol 29(1):41–49 CrossRef
- Strunk O, Ludwig W (1997) ARB: a software environment for sequence data. http://www.mikro.biologie.tu-muenchen.de
- Taiz L, Zeiger E (2006) Plant physiology. Sinauer Associates, Sunderland
- Tanner CC (1996) Plants for constructed wetland treatment systems—a comparison of the growth and nutrient uptake of eight emergent species. Ecol Eng 7:59–83 CrossRef
- Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6:579–591 CrossRef
- Thomsen TR, Kong Y, Nielsen PH (2007) Ecophysiology of abundant denitrifying bacteria in activated sludge. FEMS Microbiol Ecol 60:370–382 CrossRef
- Timmers RA, Strik DPBTB, Hamelers HVM, Buisman CJN (2010) Long-term performance of a plant microbial fuel cell with Spartina anglica. Appl Microbiol Biotechnol 86:973–981 CrossRef
- Timmers RA, Strik DPBTB, Arampatzoglou C, Buisman CJN, Hamelers HVM (2011) Rhizosphere anode model explains high oxygen levels during operation of a Glyceria maxima PMFC. Bioresource Technol. doi:10.1016/j.biortech.2011.10.088
- Van Bodegom PM, Scholten JCM (2001) Microbial processes of CH4 production in a rice paddy soil: model and experimental validation. Geochim Cosmochim Acta 65:2055–2066 CrossRef
- Xing D, Zuo Y, Cheng S, Regan JM, Logan BE (2008) Electricity generation by Rhodopseudomonas palustris DX-1. Environ Sci Technol 42:4146–4151 CrossRef
- Xing D, Cheng S, Logan BE, Regan JM (2010) Isolation of the exoelectrogenic denitrifying bacterium Comamonas denitrificans based on dilution to extinction. Appl Microbiol Biotechnol 85:1575–1587 CrossRef
About this Article
- Title
- Microbial community structure elucidates performance of Glyceria maxima plant microbial fuel cell
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
- Journal
-
Applied Microbiology and Biotechnology
Volume 94, Issue 2 , pp 537-548 - Cover Date
- 2012-04-01
- DOI
- 10.1007/s00253-012-3894-6
- Print ISSN
- 0175-7598
- Online ISSN
- 1432-0614
- Publisher
- Springer-Verlag
- Additional Links
- Topics
- Keywords
-
- 454 amplicon sequencing
- Geobacter
- Microbial community
- Plant microbial fuel cell
- Renewable energy
- Rhizosphere
- Industry Sectors
- Authors
-
- Ruud A. Timmers (1)
- Michael Rothballer (2)
- David P. B. T. B. Strik (1)
- Marion Engel (3)
- Stephan Schulz (3)
- Michael Schloter (3)
- Anton Hartmann (2)
-
Bert Hamelers
(1)
- Cees Buisman (1)
- Author Affiliations
-
- 1. Sub-department of Environmental Technology, Wageningen University, Bornseweilanden 9, 6708 WG, Wageningen, the Netherlands
- 2. Department Microbe–Plant Interactions, Helmholtz Zentrum München, German Research Center for Environmental Health, Ingolstädter Landstrasse 1, 85764, Neuherberg, Germany
- 3. Department Terrestrial Ecogenetics, Helmholtz Zentrum München, German Research Center for Environmental Health, Ingolstädter Landstrasse 1, 85764, Neuherberg, Germany