Skip to main content
SpringerLink
Log in

Magnetite production and transformation in the methanogenic consortia from coastal riverine sediments

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Minerals that contain ferric iron, such as amorphous Fe(III) oxides (A), can inhibit methanogenesis by competitively accepting electrons. In contrast, ferric iron reduced products, such as magnetite (M), can function as electrical conductors to stimulate methanogenesis, however, the processes and effects of magnetite production and transformation in the methanogenic consortia are not yet known. Here we compare the effects on methanogenesis of amorphous Fe (III) oxides (A) and magnetite (M) with ethanol as the electron donor. RNA-based terminal restriction fragment length polymorphism with a clone library was used to analyse both bacterial and archaeal communities. Iron (III)-reducing bacteria including Geobacteraceae and methanogens such as Methanosarcina were enriched in iron oxide-supplemented enrichment cultures for two generations with ethanol as the electron donor. The enrichment cultures with A and non-Fe (N) dominated by the active bacteria belong to Veillonellaceae, and archaea belong to Methanoregulaceae and Methanobacteriaceae, Methanosarcinaceae (Methanosarcina mazei), respectively. While the enrichment cultures with M, dominated by the archaea belong to Methanosarcinaceae (Methanosarcina barkeri). The results also showed that methanogenesis was accelerated in the transferred cultures with ethanol as the electron donor during magnetite production from A reduction. Powder X-ray diffraction analysis indicated that magnetite was generated from microbial reduction of A and M was transformed into siderite and vivianite with ethanol as the electron donor. Our data showed the processes and effects of magnetite production and transformation in the methanogenic consortia, suggesting that significantly different effects of iron minerals on microbial methanogenesis in the iron-rich coastal riverine environment were present.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Achtnich, C., Bak, F., and Conrad, R. 1995. Competition for electron donors among nitrate reducers, ferric iron reducers, sulfate reducers, and methanogens in anoxic paddy soil. Biol. Fertil. Soils 19, 65–72.

    Article  CAS  Google Scholar 

  • Boga, H.I., Ludwig, W., and Brune, A. 2003. Sporomusa aerivorans sp. nov., an oxygen-reducing homoacetogenic bacterium from the gut of a soil-feeding termite. Int. J. Syst. Evol. Microbiol. 53, 1397–1404.

    Article  CAS  PubMed  Google Scholar 

  • Bokulich, N.A., Bamforth, C.W., and Mills, D.A. 2012. A review of molecular methods for microbial community profiling of beer and wine. J. Am. Soc. Brew. Chem. 70, 150–162.

    CAS  Google Scholar 

  • Bond, D.R. and Lovley, D.R. 2002. Reduction of Fe(III) oxide by methanogens in the presence and absence of extracellular quinones. Environ. Microbiol. 4, 115–124.

    Article  CAS  PubMed  Google Scholar 

  • Cadillo-Quiroz, H., Yavitt, J.B., and Zinder, S.H. 2009. Methanosphaerula palustris gen. nov., sp. nov., a hydrogenotrophic methanogen isolated from a minerotrophic fen peatland. Int. J. Syst. Evol. Microbiol. 59, 928–935.

    Article  CAS  PubMed  Google Scholar 

  • Cummings, D.E., March, A.W., Bostick, B., Spring, S., Caccavo, F., Fendorf, S., and Rosenzweig, R.F. 2000. Evidence for microbial Fe (III) reduction in anoxic, mining-impacted lake sediments (Lake Coeur d’Alene, Idaho). Appl. Environ. Microbiol. 66, 154–162.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong, H.L., Fredrickson, J.K., Kennedy, D.W., Zachara, J.M., Kukkadapu, R.K., and Onstott, T.C. 2000. Mineral transformation associated with the microbial reduction of magnetite. Chem. Geol. 169, 299–318.

    Article  CAS  Google Scholar 

  • Gonnerman, M.C., Benedict, M.N., Feist, A.M., Metcalf, W.W., and Price, N.D. 2013. Genomically and biochemically accurate metabolic reconstruction of Methanosarcina barkeri Fusaro, iMG746. Biotech. J. 8, 1070–1129.

    Article  CAS  Google Scholar 

  • Hori, T., Aoyagi, T., Itoh, H., Narihiro, T., Oikawa, A., Suzuki, K., Ogata, A., Friedrich, M.W., Conrad, R., and Kamagata, Y. 2015. Isolation of microorganisms involved in reduction of crystalline iron (III) oxides in natural environments. Front. Microbiol. 6, 386.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jablonski, S., Rodowicz, P., and Lukaszewicz, M. 2015. Methanogenic archaea database containing physiological and biochemical characteristics. Int. J. Syst. Evol. Microbiol. 65, 1360–1368.

    Article  CAS  PubMed  Google Scholar 

  • Kang, Y.S., Risbud, S., Rabolt, J.F., and Stroeve, P. 1996. Synthesis and characterization of nanometer-size Fe3O4 and γ-Fe2O3 particles. Chem. Mater. 8, 2209–2211.

    Article  CAS  Google Scholar 

  • Kato, S., Hashimoto, K., and Watanabe, K. 2012a. Methanogenesis facilitated by electric syntrophy via (semi) conductive iron-oxide minerals. Environ. Microbiol. 14, 1646–1654.

    Article  CAS  PubMed  Google Scholar 

  • Kato, S., Hashimoto, K., and Watanabe, K. 2012b. Microbial interspecies electron transfer via electric currents through conductive minerals. Proc. Natl. Acad. Sci. USA 109, 10042–10046.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kern, T., Linge, M., and Rother, M. 2015. Methanobacterium aggregans sp. nov., a hydrogenotrophic methanogenic archaeon isolated from an anaerobic digester. Int. J. Syst. Evol. Microbiol. 65, 1975–1980.

    Article  CAS  PubMed  Google Scholar 

  • Kostka, J.E. and Nealson, K.H. 1995. Dissolution and reduction of magnetite by bacteria. Environ. Sci. Technol. 29, 2535–2540.

    Article  CAS  PubMed  Google Scholar 

  • Kumar, S., Stecher, G., and Tamura, K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.

    Article  CAS  PubMed  Google Scholar 

  • Li, H., Chang, J., Liu, P., Fu, L., Ding, D., and Lu, Y. 2015. Direct interspecies electron transfer accelerates syntrophic oxidation of butyrate in paddy soil enrichments. Environ. Microbiol. 17, 1533–1547.

    Article  PubMed  Google Scholar 

  • Liu, F. and Conrad, R. 2010. Thermoanaerobacteriaceae oxidize acetate in methanogenic rice field soil at 50 degrees C. Environ. Microbiol. 12, 2341–2354.

    CAS  PubMed  Google Scholar 

  • Lovley, D.R. and Phillips, E.J.P. 1986. Organic-matter mineralization with reduction of ferric iron in anaerobic sediments. Appl. Environ. Microbiol. 51, 683–689.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Oren, A. 2014. The family Methanosarcinaceae, pp. 259–281. In Rosenberg, E., De Long, E.F., Lory, S., Stackebrandt, E., and Thomson, F. The Prokaryotes. Springer Berlin, Heidelberg, Germany.

    Google Scholar 

  • Peng, Q.A., Shaaban, M., Wu, Y., Hu, R., Wang, B., and Wang, J. 2016. The diversity of iron reducing bacteria communities in subtropical paddy soils of China. Appl. Soil Ecol. 101, 20–27.

    Article  Google Scholar 

  • Piepenbrock, A., Dippon, U., Porsch, K., Appel, E., and Kappler, A. 2011. Dependence of microbial magnetite formation on humic substance and ferrihydrite concentrations. Geochim. Cosmochim. Acta 75, 6844–6858.

    Article  CAS  Google Scholar 

  • Rotaru, A.E., Shrestha, P.M., Liu, F., Markovaite, B., Chen, S., Nevin, K., and Lovley, D. 2014. Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl. Environ. Microbiol. 80, 4599–4605.

    Article  PubMed  PubMed Central  Google Scholar 

  • Schirmack, J., Mangelsdorf, K., Ganzert, L., Sand, W., Hillebrand-Voiculescu, A., and Wagner, D. 2014. Methanobacterium movilense sp. nov., a hydrogenotrophic, secondary-alcohol-utilizing methanogen from the anoxic sediment of a subsurface lake. Int. J. Syst. Evol. Microbiol. 64, 522–527.

    Article  CAS  PubMed  Google Scholar 

  • Shrestha, P.M., Kube, M., Reinhardt, R., and Liesack, W. 2009. Transcriptional activity of paddy soil bacterial communities. Environ. Microbiol. 11, 960–970.

    Article  CAS  PubMed  Google Scholar 

  • Tang, J., Zhuang, L., Ma, J., Tang, Z., Yu, Z., and Zhou, S. 2016. Secondary mineralization of ferrihydrite affects microbial methanogenesis in Geobacter-Methanosarcina cocultures. Appl. Environ. Microbiol. 82, 5869–5877.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Viggi, C.C., Rossetti, S., Fazi, S., Paiano, P., Majone, M., and Aulenta, F. 2014. Magnetite particles triggering a faster and more robust syntrophic pathway of methanogenic propionate degradation. Environ. Sci. Technol. 48, 7536–7543.

    Article  Google Scholar 

  • Yamada, C., Kato, S., Ueno, Y., Ishii, M., and Igarashi, Y. 2014. Inhibitory effects of ferrihydrite on a thermophilic methanogenic community. Microbes Environ. 29, 227–230.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang, Z.M., Shi, X.S., Wang, C.S., Wang, L., and Guo, R.B. 2015. Magnetite nanoparticles facilitate methane production from ethanol via acting as electron acceptors. Sci. Rep. 5, 16118.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, J., Dong, H.L., Liu, D., Fischer, T.B., Wang, S., and Huang, L.Q. 2012. Microbial reduction of Fe(III) in illite-smectite minerals by methanogen Methanosarcina mazei. Chem. Geol. 292, 35–44.

    Article  Google Scholar 

  • Zheng, S., Zhang, H., Li, Y., Zhang, H., Wang, O., Zhang, J., and Liu, F. 2015. Co-occurrence of Methanosarcina mazei and Geobacteraceae in an iron (III)-reducing enrichment culture. Front. Microbiol. 6, 941.

    PubMed  PubMed Central  Google Scholar 

  • Zhou, S., Xu, J., Yang, G., and Zhuang, L. 2014. Methanogenesis affected by the co-occurrence of iron (III) oxides and humic substances. FEMS Microbiol. Ecol. 88, 107–120.

    Article  CAS  PubMed  Google Scholar 

  • Zhuang, L., Xu, J.L., Tang, J., and Zhou, S.G. 2015. Effect of ferrihydrite biomineralization on methanogenesis in an anaerobic incubation from paddy soil. J. Geophys. Res. Biogeosci. 120, 876–886.

    Article  CAS  Google Scholar 

Download references

Author information

Author notes

  1. These authors contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Coastal Biology and Biological Resources Utilization, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, 264003, P. R. China

    Shiling Zheng, Bingchen Wang & Fanghua Liu

  2. University of Chinese Academy of Sciences, Beijing, 100049, P. R. China

    Bingchen Wang

  3. Binzhou Medical University, Yantai, 264003, P. R. China

    Oumei Wang

Authors
  1. Shiling Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bingchen Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fanghua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Oumei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Fanghua Liu or Oumei Wang.

Additional information

Supplemental material for this article may be found at http://www.springerlink.com/content/120956.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zheng, S., Wang, B., Liu, F. et al. Magnetite production and transformation in the methanogenic consortia from coastal riverine sediments. J Microbiol. 55, 862–870 (2017). https://doi.org/10.1007/s12275-017-7104-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-017-7104-1

Keywords

Search

Navigation