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The influence of soil properties and geographical distance on the bacterial community compositions of paddy soils enriched on SMFC anodes

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
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Abstract

Purpose

Exoelectrogens are important microorganisms playing crucial roles in the biogeochemistry of elements in paddy soils. But it remains unclear how the soil properties and geographical distances affect the exoelectrogen communities of Chinese paddy soils. So the objectives of this study were to investigate the diversity and composition of these microbial communities which were enriched on the anodes of soil microbial fuel cells (SMFCs) and to elucidate the links between the microbial community compositions and their driving factors.

Materials and methods

We used Illumina HiSeq sequencing to determine the bacterial community structures which were enriched on the anodes of SMFCs. Variance partitioning analysis (VPA) was used to obtain the contribution of soil properties and geographical distance to the variations of bacterial communities.

Results and discussion

Active bacterial community on anodes of the closed circuit SMFCs differs significantly from the control open circuit SMFCs. Anodes of all the closed circuit SMFCs were characterized by the presence of high numbers of Nitrospira and Anaerolineae. Taxonomic similarities and phylogenetic similarities of bacterial communities from different paddy soil samples across North and South China were found to be significantly correlated with geographical distances. The relationship between the similarities and the geographic distance exhibited a distance-decay relationship. VPA showed that both geographical distances and soil properties affect the structure of bacterial communities detected on anodes.

Conclusions

Our study gives a foundation for understanding the distribution and diversity of exoelectrogens in paddy soils and elucidates the links between the distribution and the diversity of extracellular respiring bacteria and their driving factors. Furthermore, this study also identifies the crucial factors which should be used to evaluate the response of exoelectrogens to environmental perturbations in Chinese paddy soils.

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References

  • Aelterman P, Freguia S, Keller J, Verstraete W, Rabaey K (2008) The anode potential regulates bacterial activity in microbial fuel cells. Appl Microbiol Biot 78:409–418

    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 

  • Brutinel ED, Gralnick JA (2012) Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biot 93:41–48

    Article  Google Scholar 

  • Carroll IM, Ringel-Kulka T, Siddle JP, Ringel Y (2012) Alterations in composition and diversity of the intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Neurogastroent Motil 24:521–e248

    Article  CAS  Google Scholar 

  • Chen S, Tang J, Fu L, Yuan Y, Zhou S (2016) Biochar improves sediment microbial fuel cell performance in low conductivity freshwater sediment. J Soils Sediments 16:2326–2334

    Article  CAS  Google Scholar 

  • Chu H, Fierer N, Lauber CL, Caporaso J, Knight R, Grogan P (2010) Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ Microbiol 12:2998–3006

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ding L-J, Su J-Q, Xu H-J, Jia Z-J, Zhu Y-G (2015) Long-term nitrogen fertilization of paddy soil shifts iron-reducing microbial community revealed by RNA-13C-acetate probing coupled with pyrosequencing. ISME J 9:721–734

    Article  CAS  Google Scholar 

  • Doyle LE, Marsili E (2015) Methods for enrichment of novel electrochemically-active microorganisms. Bioresour Technol 195:273–282

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Feng Y, Grogan P, Caporaso JG, Zhang H, Lin X, Knight R, Chu H (2014) pH is a good predictor of the distribution of anoxygenic purple phototrophic bacteria in Arctic soils. Soil Biol Biochem 74:193–200

    Article  CAS  Google Scholar 

  • Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. P Natl Acad Sci USA 103:626–631

    Article  CAS  Google Scholar 

  • Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL (2008) Towards environmental systems biology of Shewanella. Nat Rev Microbiol 6:592–603

    Article  CAS  Google Scholar 

  • Ge Y, He J-Z, Zhu Y-G, Zhang J-B, Xu Z, Zhang L-M, Zheng Y-M (2008) Differences in soil bacterial diversity: driven by contemporary disturbances or historical contingencies? ISME J 2:254–264

    Article  CAS  Google Scholar 

  • Girguis PR, Nielsen ME, Figueroa I (2010) Harnessing energy from marine productivity using bioelectrochemical systems. Curr Opin Biotech 21:252–258

    Article  CAS  Google Scholar 

  • Goto Y, Yoshida N, Umeyama Y, Yamada T, Tero R, Hiraishi A (2015) Enhancement of electricity production by graphene oxide in soil microbial fuel cells and plant microbial fuel cells. Front Bioeng Biotechnol 3:1–8

    Article  Google Scholar 

  • Griffiths RI, Thomson BC, James P, Bell T, Bailey M, Whiteley AS (2011) The bacterial biogeography of British soils. Environ Microbiol 13:1642–1654

    Article  Google Scholar 

  • Hau HH, Gralnick JA (2007) Ecology and biotechnology of the genus Shewanella. Annu Rev Microbiol 61:237–258

    Article  CAS  Google Scholar 

  • Holmes DE, O'Neil RA, Vrionis HA, N'guessan LA, Ortiz-Bernad I, Larrahondo MJ, Adams LA, Ward JA, Nicoll JS, Nevin KP (2007) Subsurface clade of Geobacteraceae that predominates in a diversity of Fe(III)-reducing subsurface environments. ISME J 1:663–677

    Article  CAS  Google Scholar 

  • Huang L, Regan JM, Quan X (2011) Electron transfer mechanisms, new applications, and performance of biocathode microbial fuel cells. Bioresour Technol 102:316–323

    Article  CAS  Google Scholar 

  • Ishii S, Shimoyama T, Hotta Y, Watanabe K (2008a) Characterization of a filamentous biofilm community established in a cellulose-fed microbial fuel cell. BMC Microbiol 8:1–12

    Article  Google Scholar 

  • Ishii S, Watanabe K, Yabuki S, Logan BE, Sekiguchi Y (2008b) Comparison of electrode reduction activities of Geobacter sulfurreducens and an enriched consortium in an air-cathode microbial fuel cell. Appl Environ Microbiol 74:7348–7355

    Article  CAS  Google Scholar 

  • Ishii S, Suzuki S, Norden-Krichmar TM, Nealson KH, Sekiguchi Y, Gorby YA, Bretschger O (2012) Functionally stable and phylogenetically diverse microbial enrichments from microbial fuel cells during wastewater treatment. PLoS One 7:e30495

    Article  CAS  Google Scholar 

  • Ishii S, Suzuki S, Norden-Krichmar TM, Phan T, Wanger G, Nealson KH, Sekiguchi Y, Gorby YA, Bretschger O (2014) Microbial population and functional dynamics associated with surface potential and carbon metabolism. ISME J 8:963–978

    Article  CAS  Google Scholar 

  • Kia E, Mackenzie BW, Middleton D, Lau A, Waite DW, Lewis G, Chan Y-K, Silvestre M, Cooper GJ, Poppitt SD (2016) Integrity of the human faecal microbiota following long-term sample storage. PLoS One 11:e0163666

    Article  Google Scholar 

  • Kiely PD, Regan JM, Logan BE (2011) The electric picnic: synergistic requirements for exoelectrogenic microbial communities. Curr Opin Biotech 22:378–385

    Article  CAS  Google Scholar 

  • Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120

    Article  CAS  Google Scholar 

  • Li H, Peng J, Weber KA, Zhu Y (2011) Phylogenetic diversity of Fe(III)-reducing microorganisms in rice paddy soil: enrichment cultures with different short-chain fatty acids as electron donors. J Soils Sediments 11:1234–1242

    Article  CAS  Google Scholar 

  • Liesack W, Schnell S, Revsbech NP (2000) Microbiology of flooded rice paddies. FEMS Microbiol Rev 24:625–645

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286

    Article  CAS  Google Scholar 

  • Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei T, Damsté JSS, Spieck E, Le Paslier D (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. P Natl Acad Sci USA 107:13479–13484

    Article  Google Scholar 

  • Martiny JB, Eisen JA, Penn K, Allison SD, Horner-Devine MC (2011) Drivers of bacterial β-diversity depend on spatial scale. P Natl Acad Sci USA 108:7850–7854

    Article  CAS  Google Scholar 

  • Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30:3123–3124

    Article  CAS  Google Scholar 

  • Puig S, Serra M, Coma M, Cabré M, Balaguer MD, Colprim J (2010) Effect of pH on nutrient dynamics and electricity production using microbial fuel cells. Bioresour Technol 101:9594–9599

    Article  CAS  Google Scholar 

  • Rodrigues JL, Pellizari VH, Mueller R, Baek K, Jesus EC, Paula FS, Mirza B, Hamaoui GS, Tsai SM, Feigl B (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. P Natl Acad Sci USA 110:988–993

    Article  CAS  Google Scholar 

  • Sajana T, Ghangrekar M, Mitra A (2016) In situ bioremediation using sediment microbial fuel cell. J Hazard Toxic Radioact Waste 12(2):04016022

    Google Scholar 

  • Scheibe A, Steffens C, Seven J, Jacob A, Hertel D, Leuschner C, Gleixner G (2015) Effects of tree identity dominate over tree diversity on the soil microbial community structure. Soil Biol Biochem 81:219–227

    Article  CAS  Google Scholar 

  • Shi L, Dong H, Reguera G, Beyenal H, Lu A, Liu J, Yu H-Q, Fredrickson JK (2016) Extracellular electron transfer mechanisms between microorganisms and minerals. Nature Rev Microbiol 14:651–662

    Article  CAS  Google Scholar 

  • Wang N, Chen Z, Li H-B, Su J-Q, Zhao F, Zhu Y-G (2015) Bacterial community composition at anodes of microbial fuel cells for paddy soils: the effects of soil properties. J Soils Sediments 15:926–936

    Article  CAS  Google Scholar 

  • Weelink SA, Van Doesburg W, Saia FT, Rijpstra WIC, Röling WF, Smidt H, Stams AJ (2009) A strictly anaerobic betaproteobacterium Georgfuchsia toluolica gen. nov., sp. nov. degrades aromatic compounds with Fe(III), Mn(IV) or nitrate as an electron acceptor. FEMS Microbiol Ecol 70:575–585

    Article  CAS  Google Scholar 

  • Xia Z, Bai E, Wang Q, Gao D, Zhou J, Jiang P, Wu J (2016) Biogeographic distribution patterns of bacteria in typical Chinese forest soils. Front Microbiol 7:1106

    Article  Google Scholar 

  • Yamada T, Sekiguchi Y (2009) Cultivation of uncultured chloroflexi subphyla: significance and ecophysiology of formerly uncultured chloroflexi ’subphylum I’ with natural and biotechnological relevance. Microb Environ 24:205–216

    Article  Google Scholar 

  • Yang WH, Weber KA, Silver WL (2012) Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nat Geosci 5:538–541

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Yuan H-Y, Ding L-J, Wang N, Chen S-C, Deng Y, Li X-M, Zhu Y-G (2016) Geographic distance and amorphous iron affect the abundance and distribution of Geobacteraceae in paddy soils in China. J Soils Sediments 16:2657–2665

    Article  CAS  Google Scholar 

  • Zhang S-Y, Zhao F-J, Sun G-X, Su J-Q, Yang X-R, Li H, Zhu Y-G (2015) Diversity and abundance of arsenic biotransformation genes in paddy soils from Southern China. Environ Sci Technol 49:4138–4146

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (41430858) and the Strategic Priority Research Program of Chinese Academy of Sciences (XDB15020402).

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Correspondence to Guo-Xin Sun.

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Responsible editor: Huaiying Yao

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Yuan, HY., Liu, PP., Wang, N. et al. The influence of soil properties and geographical distance on the bacterial community compositions of paddy soils enriched on SMFC anodes. J Soils Sediments 18, 517–525 (2018). https://doi.org/10.1007/s11368-017-1769-2

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  • DOI: https://doi.org/10.1007/s11368-017-1769-2

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