Anode electrogenic bacteria (AEB) widely exist in paddy soils and play an important role in element biogeochemical cycling. However, little information is available on the role of soil characteristics in shaping AEB community. Therefore, the objective of this study was to evaluate the role of soil properties in driving the evolution of anode bacterial communities.
Materials and methods
Microbial fuel cells (MFCs) were constructed for five paddy soils with different chemical properties. The bacterial communities at anodes of closed (MFC running) and open (control) circuit MFCs were characterized using 16S rRNA gene-based Illumina sequencing.
Results and discussion
Paddy soils with higher dissolved organic carbon (DOC) and ammonium (NH4 +) concentrations in porewater showed higher MFC performance. Without MFC running, the dominant bacterial community composition was similar among the used five soils with Clostridia as the dominant bacteria at class level. Compared to control treatments, MFC running significantly decreased bacterial diversity and altered the bacterial community composition at anodes. However, the shift of bacterial communities varied with different types of soils. Betaproteobacteria was enriched by 4–30 times after MFC running for low MFC performance soils, while Deltaproteobacteria enriched (4–20 times) for high MFC performance soils. Redundancy analysis (RDA) indicated that DOC, NH4 +, and dissolved ferrous (Fe2+) significantly shift anode bacterial communities for the five soils with MFC running.
We found that high-performing MFCs constructed from paddy soils with high DOC and NH4 + concentrations in porewater selected for an active, highly electrogenic bacterial community (dominated by Deltaproteobacteria) at anodes, while the dominant bacterial community for the low-performing MFCs from soils with low DOC and NH4 + was Betaproteobacteria. These findings imply that soil properties shape the AEB composition, therefore influencing MFC performance. This study provides new insights into the microbial-mediated carbon and nitrogen cycling in paddy soils.
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Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
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
Chen Z, Huang YC, Liang JH, Zhao F, Zhu YG (2012) A novel sediment microbial fuel cell with a biocathode in the rice rhizosphere. Bioresour Technol 108:55–59
Clément JC, Shrestha J, Ehrenfeld JG, Jaffé PR (2005) Ammonium oxidation coupled to dissimilatory reduction of iron under anaerobic conditions in wetland soils. Soil Biol Biochem 37:2323–2328
Da Rosa AC (2010) Diversity and function of the microbial community on anodes of sediment microbial fuel cells fueled by root exudates. Dissertation, Philipps-Universität Marburg
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(6):2002–2008
Ding LJ, An XL, Li S, Zhang GL, Zhu YG (2014) Nitrogen loss through anaerobic ammonium oxidation coupled to iron reduction from paddy soils in a chronosequence. Environ Sci Technol 48(18):10641–10647
Domínguez-Garay A, Berná A, Ortiz-Bernad I, Esteve-Núñez A (2013) Silica colloid formation enhances performance of sediment microbial fuel cells in a low conductivity soil. Environ Sci Technol 47:2117–2122
Dumas C, Mollica A, Feron D, Basseguy R, Etcheverry L, Bergel A (2008) Checking graphite and stainless anodes with an experimental model of marine microbial fuel cell. Bioresour Technol 99(18):8887–8894
Dunaj SJ, Vallino JJ, Hines ME, Gay M, Kobyljanec C, Rooney-Varga JN (2012) Relationships between soil organic matter, nutrients, bacterial community structure, and the performance of microbial fuel cells. Environ Sci Technol 46:1914–1922
Esteve-Núñez A, Sosnik J, Visconti P, Lovley DR (2008) Fluorescent properties of c-type cytochromes reveal their potential role as an extracytoplasmic electron sink in Geobacter sulfurreducens. Environ Microbiol 10:497–505
Hamady M, Walker JJ, Harris JK, Gold NJ, Knight R (2008) Error-correcting barcoded primers for pyrosequencing hundreds of samples in multiplex. Nat Methods 5:235–237
He Z, Kan J, Wang Y, Huang Y, Mansfeld F, Nealson KH (2009) Electricity production coupled to ammonium in a microbial fuel cell. Environ Sci Technol 43:3391–3397
Hobbie SN, Li XZ, Basen M, Stingl U, Brune A (2012) Humic substance-mediated Fe(III) reduction by a fermenting Bacillus strain from the alkaline gut of a humus-feeding scarab beetle larva. Syst Appl Microbiol 35:226–232
Huse SM, Dethlefsen L, Huber JA, Welch DM, Relman DA, Sogin ML (2008) Exploring microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing. Plos Genet 4:e1000255
Institute of Soil Science, Chinese of Academy of Sciences (1978) Soils of China (in Chinese). Science Press, Beijing
Islam FS, Gault AG, Boothman C, Polya DA, Charnock JM, Chatterjee D, Lloyd JR (2004) Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 430(6995):68–71
Jetten MS, Strous M, Pas‐Schoonen KT, Schalk J, Dongen UG, Graaf AA, Logemann S, Muyzer G, Loosdrecht M, Kuenen JG (1998) The anaerobic oxidation of ammonium. FEMS Microbiol Rev 22:421–437
Jung S, Regan JM (2011) Influence of external resistance on electrogenesis, methanogenesis, and anode prokaryotic communities in microbial fuel cells. Appl Environ Microbiol 77(2):564–571
Kaku N, Yonezawa N, Kodama Y, Watanabe K (2008) Plant/microbe cooperation for electricity generation in a rice paddy field. Appl Microbiol Biotechnol 79(1):43–49
Kan J, Hsu L, Cheung AC, Pirbazari M, Nealson KH (2010) Current production by bacterial communities in microbial fuel cells enriched from wastewater sludge with different electron donors. Environ Sci Technol 45:1139–1146
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(6):672–681
Kim GT, Webster G, Wimpenny JWT, Kim BH, Kim HJ, Weightman AJ (2006) Bacterial community structure, compartmentalization and activity in a microbial fuel cell. J Appl Microbiol 101(3):698–710
Kögel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Kölbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157(1):1–14
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
Li Z, Haynes R, Stato F, Shield MS, Fujita Y, Stao C (2014) Microbial community analysis of a single chamber microbial fuel cell using potato wastewater. Water Environ Res 86:324–330
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
Logan BE, Regan JM (2006) Electricity-producing bacterial communities in microbial fuel cells. Trends Microbiol 14:512–518
Lovley DR (1997) Microbial Fe (III) reduction in subsurface environments. FEMS Microbiol Rev 20(3–4):305–313
Lovley DR (2006) Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4:497–508
Lovley DR (2013) Dissimilatory Fe(III)- and Mn(IV)-reducing prokaryotes. In: The prokaryotes. Springer Berlin Heidelberg, pp 287–308
Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235
Lozupone C, Hamady M, Knight R (2006) UniFrac—an online tool for comparing microbial community diversity in a phylogenetic context. Bmc Bioinforma 7(1):371
Miceli JF III, Parameswaran P, Kang DW, Krajmalnik-Brown R, Torres CI (2012) Enrichment and analysis of anode-respiring bacteria from diverse anaerobic inocula. Environ Sci Technol 46:10349–10355
Mou S, Wang H, Sun Q (1993) Simultaneous determination of the three main inorganic forms of nitrogen by ion chromatography. J Chromatogr A 640:161–165
Oksanen J (2013) Multivariate analysis of ecological communities in R: vegan tutorial. R Packag Version 2.0–10:18–30
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(1):77–82
Raiswell R, Canfield DE (2012) The iron biogeochemical cycle past and present. Geochem Perspect 1(1):1–2
Ryckelynck N, Stecher HA III, Reimers CE (2005) Understanding the anodic mechanism of a seafloor fuel cell: interactions between geochemistry and microbial activity. Biogeochemistry 76(1):113–139
Scala DJ, Hacherl EL, Cowan R, Young LY, Kosson DS (2006) Characterization of Fe(III)-reducing enrichment cultures and isolation of Fe(III)-reducing bacteria from the Savannah River site, South Carolina. Res Microbiol 157(8):772–783
Scott DT, McKnight DM, Blunt-Harris EL, Kolesar SE, Lovley DR (1998) Quinone moieties act as electron acceptors in the reduction of humic substances by humics-reducing microorganisms. Environ Sci Technol 32(19):2984–2989
Schaetzle O, Barrière F, Baronian K (2008) Bacteria and yeasts as catalysts in microbial fuel cells: electron transfer from micro-organisms to electrodes for green electricity. Energy Environ Sci 1(6):607–620
Shanh M, Lin CC, Kukkadapu R, Engelhard MH, Zhao X, Wang YP, Barkey T, Yee N (2014) Syntrophic effects in a subsurface clostridial consortium on Fe(III)-(Oxyhydr) oxide reduction and secondary mineralization. Geomicrobiol J 31(2):101–115
Shrestha PM, Rotaru AE, Aklujkar M, Liu F, Shrestha M, Summers ZM, Lovley DR (2013) Syntrophic growth with direct interspecies electron transfer as the primary mechanism for energy exchange. Environ Microbiol Rep 5(6):904–910
Stams AJ, Plugge CM (2009) Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol 7:568–577
Stookey LL (1970) Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42:779–781
Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330:1413–1415
Takanezawa K, Nishio K, Kato S, Hashimoto K, Watanabe K (2010) Factors affecting electric output from rice-paddy microbial fuel cells. Biosci Biotechnol Biochem 74(6):1271–1273
Thamdrup B (2000) Bacterial manganese and iron reduction in aquatic sediments. In: Advances in microbial ecology. Springer US, pp 41–84
Tender LM, Reimers CE, Stecher HA, 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
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267
Wang XJ, Yang J, Chen XP, Sun GX, Zhu YG (2009) Phylogenetic diversity of dissimilatory ferric iron reducers in paddy soil of Hunan, South China. J Soils Sediments 9(6):568–577
Weber KA, Urrutia MM, Churchill PF, Kukkadapu RK, Roden EE (2006) Anaerobic redox cycling of iron by freshwater sediment microorganisms. Environ Microbiol 8:100–113
Wrighton KC, Coates JD (2009) Microbial fuel cells: plug-in and power-on microbiology. Microbe 4(6):281–287
Yates MD, Kiely PD, Call DF, Rismani-Yazdi H, Bibby K, Peccia J, Regan JM, Logan BE (2012) Convergent development of anodic bacterial communities in microbial fuel cells. Isme J 6:2002–2013
Yi W, You J, Zhu C, Wang B, Qu D (2013) Diversity, dynamic and abundance of Geobacteraceae species in paddy soil following slurry incubation. Eur J Soil Biol 56:11–18
Zhu XP, Yates MD, Logan BE (2012) Set potential regulation reveals additional oxidation peaks of Geobacter sulfurreducens anodic biofilms. Electrochem Commun 22:116–119
Our research is supported by the National Natural Science foundation of China (41090282 and 41430858) and the International Collaboration Program (2011DFB91710).
Responsible editor: Chengrong Chen
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Wang, N., Chen, Z., Li, H. et al. Bacterial community composition at anodes of microbial fuel cells for paddy soils: the effects of soil properties. J Soils Sediments 15, 926–936 (2015). https://doi.org/10.1007/s11368-014-1056-4
- Anode electrogenic bacteria (AEB)
- Illumina sequencing
- Microbial fuel cells
- Paddy soil