Skip to main content
SpringerLink
Log in

Extraction of electrons by magnetite and ferrihydrite from hydrogen-producing Clostridium bifermentans by strengthening the acetate production pathway

  • Article
  • Published:
Science China Technological Sciences Aims and scope Submit manuscript

Abstract

Conductive mineral nanoparticles, such as magnetite, can promote interspecies electron transfer between syntrophic partners. However, the effect of magnetite has only been inferred in intraspecific electron output. Herein, a hydrogen-producing strain, namely, Clostridium bifermentans, which holds several electron output pathways, was used to study the effect of magnetite on the intraspecific electron output manner. Additionally, insulated amorphous ferrihydrite, which was used as an extracellular electron acceptor, was selected to compare with magnetite. Electrons, which were originally used to generate hydrogen, were shunted with the addition of magnetite and ferrihydrite, which resulted in the reduction of hydrogen production and accumulation of Fe(II). Interestingly, more electrons (39.7% and 53.5%) were extracted by magnetite and ferrihydrite, respectively, which led to less production of butyrate and more acetate. More importantly, the increased electron extraction efficiency suggested that electroactive microorganisms can switch metabolic pathways to adapt to electron budget pressure in intraspecific systems. This work broadens the understanding of the interaction between iron oxides and fermentative hydrogen-producing microbes that hold the capacity of Fe(III) reduction.

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

  1. Lovley D R. Dissimilatory metal reduction: From early life to bior-emediation. Asm News, 2002, 68: 231–237

    Google Scholar 

  2. Nealson K H, Saffarini D. Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. Annu Rev Microbiol, 1994, 48: 311–343

    Article  Google Scholar 

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

    Google Scholar 

  4. Show K Y, Lee D J, Tay J H, et al. Biohydrogen production: Current perspectives and the way forward. Int J Hydrogen Energy, 2012, 37: 15616–15631

    Article  Google Scholar 

  5. Jelen B I, Giovannelli D, Falkowski P G. The role of microbial electron transfer in the coevolution of the biosphere and geosphere. Annu Rev Microbiol, 2016, 70: 45–62

    Article  Google Scholar 

  6. Byrne J M, Klueglein N, Pearce C, et al. Redox cycling of Fe(II) and Fe(III) in magnetite by Fe-metabolizing bacteria. Science, 2015, 347: 1473–1476

    Article  Google Scholar 

  7. Xiao L, Liu F, Liu J, et al. Nano-Fe3O4 particles accelerating electromethanogenesis on an hour-long timescale in wetland soil. Environ Sci-Nano, 2018, 5: 436–445

    Article  Google Scholar 

  8. Bose A, Gardel E J, Vidoudez C, et al. Electron uptake by iron-oxidizing phototrophic bacteria. Nat Commun, 2014, 5: 3391

    Article  Google Scholar 

  9. Shelobolina E, Xu H, Konishi H, et al. Microbial lithotrophic oxidation of structural Fe(II) in biotite. Appl Environ Microbiol, 2012, 78: 5746–5752

    Article  Google Scholar 

  10. Lovley D R, Phillips E J P. Novel mode of microbial energy-metabolism-organic-carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microb, 1988, 54: 1472–1480

    Google Scholar 

  11. Gadhe A, Sonawane S S, Varma M N. Enhancement effect of hematite and nickel nanoparticles on biohydrogen production from dairy was-tewater. Int J Hydrogen Energy, 2015, 40: 4502–4511

    Article  Google Scholar 

  12. Han H, Cui M, Wei L, et al. Enhancement effect of hematite nano-particles on fermentative hydrogen production. Bioresource Tech, 2011, 102: 7903–7909

    Article  Google Scholar 

  13. Reddy K, Nasr M, Kumari S, et al. Biohydrogen production from sugarcane bagasse hydrolysate: Effects of pH, S/X, Fe2+, and magnetite nanoparticles. Environ Sci Pollut Res, 2017, 24: 8790–8804

    Article  Google Scholar 

  14. Mohanraj S, Kodhaiyolii S, Rengasamy M, et al. Phytosynthesized iron oxide nanoparticles and ferrous iron on fermentative hydrogen production using Enterobacter cloacae: Evaluation and comparison of the effects. Int J Hydrogen Energy, 2014, 39: 11920–11929

    Article  Google Scholar 

  15. Nasr M, Tawfik A, Ookawara S, et al. Continuous biohydrogen production from starch wastewater via sequential dark-photo fermentation with emphasize on maghemite nanoparticles. J Industrial Eng Chem, 2015, 21: 500–506

    Article  Google Scholar 

  16. Dalla Vecchia E, Suvorova E I, Maillard J, et al. Fe(III) reduction during pyruvate fermentation by Desulfotomaculum reducens strain MI-1. Geobiology, 2014, 12: 48–61

    Article  Google Scholar 

  17. Dong Y, Sanford R A, Chang Y J, et al. Hematite reduction buffers acid generation and enhances nutrient uptake by a fermentative iron reducing bacterium, Orenia metallireducens Strain Z6. Environ Sci Tech, 2017, 51: 232–242

    Article  Google Scholar 

  18. Park H S, Kim B H, Kim H S, et al. A novel electrochemically active and Fe(III)-reducing bacterium phylogenetically related to Clostridium butyricum isolated from a microbial fuel cell. Anaerobe, 2001, 7: 297–306

    Article  Google Scholar 

  19. Zhang Y, Xiao L, Wang O, et al. Hydrogen-producing and electrochemical properties of a dissimilatory Fe(III) reducer Clostridium bifermentans EZ-1. Acta Microbio Sin, 2018, 4: 525–537

    Google Scholar 

  20. Xiao L, Xie B, Liu J, et al. Stimulation of long-term ammonium nitrogen deposition on methanogenesis by Methanocellaceae in a coastal wetland. Sci Total Environ, 2017, 595: 337–343

    Article  Google Scholar 

  21. Lee J, Jung N, Shin J H, et al. Enhancement of hydrogen production and power density in a bio-reformed formic acid fuel cell (BrFAFC) using genetically modified Enterobacter asburiae SNU-1. Int J Hydrogen Energy, 2014, 39: 11731–11737

    Article  Google Scholar 

  22. Lovley D R, Phillips E J P. Availability of ferric iron for microbial reduction in bottom sediments of the fresh-water tidal potomac river. Appl Environ Microb, 1986, 52: 751–757

    Google Scholar 

  23. Kang Y S, Risbud S, Rabolt J F, et al. Synthesis and characterization of nanometer-size Fe3O4 and γ-Fe2O3 particles. Chem Mater, 1996, 8: 2209–2211

    Article  Google Scholar 

  24. Stookey L L. Ferrozine—a new spectrophotometric reagent for iron. Anal Chem, 1970, 42: 779–781

    Article  Google Scholar 

  25. Weisener C G, Guthrie J W, Smeaton C M, et al. The effect of Ca-Fe-As coatings on microbial leaching of metals in arsenic bearing mine waste. J GeoChem Exploration, 2011, 110: 23–30

    Article  Google Scholar 

  26. Ishii S, Watanabe K, Yabuki S, et al. Comparison of electrode reduction activities of Geobacter sulfurreducens and an enriched Consortium in an air-cathode microbial fuel cell. Appl Environ MicroBiol, 2008, 74: 7348–7355

    Article  Google Scholar 

  27. Li J, Xiao L, Zheng S, et al. A new insight into the strategy for methane production affected by conductive carbon cloth in wetland soil: Beneficial to acetoclastic methanogenesis instead of CO2 reduction. Sci Total Environ, 2018, 643: 1024–1030

    Article  Google Scholar 

  28. Hsieh P H, Lai Y C, Chen K Y, et al. Explore the possible effect of TiO2 and magnetic hematite nanoparticle addition on biohydrogen production by Clostridium pasteurianum based on gene expression measurements. Int J Hydrogen Energy, 2016, 41: 21685–21691

    Article  Google Scholar 

  29. Wu H, Wang C, Chen P, et al. Corrigendum to “Effects of pH and ferrous iron on the coproduction of butanol and hydrogen by Clostridium beijerinckii IB4” [Int J Hydrogen Energy 42 (2017) 6547–6555]. Int J Hydrogen Energy, 2017, 42: 20399

    Article  Google Scholar 

  30. Beckers L, Hiligsmann S, Lambert S D, et al. Improving effect of metal and oxide nanoparticles encapsulated in porous silica on fermentative biohydrogen production by Clostridium butyricum. Bioresource Tech, 2013, 133: 109–117

    Article  Google Scholar 

  31. Dobbin P S, Carter J P, Garcäa-Salamanca San Juan C, et al. Dissimilatory Fe(III) reduction by Clostridium beijerinckii isolated from freshwater sediment using Fe(III) maltol enrichment. FEMS Micro-Biol Lett, 1999, 176: 131–138

    Article  Google Scholar 

  32. Abdeshahian P, Al-Shorgani N K N, Salih N K M, et al. The production of biohydrogen by a novel strain Clostridium sp. YM1 in dark fermentation process. Int J Hydrogen Energy, 2014, 39: 12524–12531

    Article  Google Scholar 

  33. Lehours A C, Rabiet M, Morel-Desrosiers N, et al. Ferric iron reduction by fermentative strain BS2 isolated from an iron-rich anoxic environment (Lake Pavin, France). GeomicroBiol J, 2010, 27: 714–722

    Article  Google Scholar 

  34. Liang B, Cheng H Y, Kong D Y, et al. Accelerated reduction of chlorinated nitroaromatic antibiotic chloramphenicol by biocathode. Environ Sci Technol, 2013, 47: 5353–5361

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant Nos. 91751112, 41573071, 41703075, 41807325), the Senior User Project of RV KEXUE (Grant No. KEXUE2018G01), the Key Research Project of Frontier Science (Grant No. QYZDJ-SSW-DQC015) of the Chinese Academy of Sciences, the Natural Science Foundation (Grant Nos. JQ201608, ZR2016DQ12), and the Young Taishan Scholars Program (Grant No. tsqn20161054) of Shandong Province.

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, China

    YueChao Zhang, FangHua Liu, HengDuo Xu & LeiLei Xiao

  2. Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266237, China

    YueChao Zhang & FangHua Liu

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    YueChao Zhang

Authors
  1. YueChao Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. FangHua Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. HengDuo Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. LeiLei Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to FangHua Liu or LeiLei Xiao.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Liu, F., Xu, H. et al. Extraction of electrons by magnetite and ferrihydrite from hydrogen-producing Clostridium bifermentans by strengthening the acetate production pathway. Sci. China Technol. Sci. 62, 1719–1725 (2019). https://doi.org/10.1007/s11431-018-9460-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11431-018-9460-9

Search

Navigation