Skip to main content
Log in

Ecological responses to substrates in electroactive biofilm: A review

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

Abstract

Substrate as the electron donor of bioelectrochemical system (BES) has fateful impacts on the microbial community composition of electroactive biofilm (EAB), via the selection upon functional microorganisms such as exoelectrogens, fermenters and methanogens, as well as their interactions. Electrochemical performance as the terminal reflects of electroactivity and the correspondence between community members have been summarized. Exoelectrogens responsible to the conversion towards electricity from their respective preferred substrates such as acetate, propionate, glucose and cellulose has been found to be finite in a small range, e.g., Geobacter, Shewanella and Pseudomonas. Their demands of micromolecular electron donors and the selective pressure of primary substrates facilitate the existence of competitive or cooperative biological processes to exoelectrogenesis. The inherent mechanisms of the dynamics of such interactions have been explored with electrochemical methods, defined co-culture experiments and community analysis. Complete view of the metabolic network in electroactive microbial communities has been shed light on, and appeals further investigation.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Gadkari S, Gu S, Sadhukhan J. Towards automated design of bioelectrochemical systems: A comprehensive review of mathematical models. Chem Eng J, 2018, 343: 303–316

    Google Scholar 

  2. Harnisch F, Schröder U. From MFC to MXC: Chemical and biological cathodes and their potential for microbial bioelectrochemical systems. Chem Soc Rev, 2010, 39: 4433

    Google Scholar 

  3. Wang H, Ren Z J. A comprehensive review of microbial electrochemical systems as a platform technology. Biotech Adv, 2013, 31: 1796–1807

    Google Scholar 

  4. Pant D, Singh A, Van Bogaert G, et al. Bioelectrochemical systems (BES) for sustainable energy production and product recovery from organic wastes and industrial wastewaters. RSC Adv, 2012, 2: 1248–1263

    Google Scholar 

  5. Pous N, Carmona-Martínez A A, Vilajeliu-Pons A, et al. Bidirectional microbial electron transfer: Switching an acetate oxidizing biofilm to nitrate reducing conditions. Biosens Bioelectron, 2016, 75: 352–358

    Google Scholar 

  6. Kumar A, Hsu L H H, Kavanagh P, et al. The ins and outs of microorganism-electrode electron transfer reactions. Nat Rev Chem, 2017, 1: 0024

    Google Scholar 

  7. Yang G, Huang L, You L, et al. Electrochemical and spectroscopic insights into the mechanisms of bidirectional microbe-electrode electron transfer in Geobacter soli biofilms. Electrochem Commun, 2017, 77: 93–97

    Google Scholar 

  8. Shi L, Squier T C, Zachara J M, et al. Respiration of metal (hydr) oxides by Shewanella and Geobacter: A key role for multihaem c-type cytochromes. Mol MicroBiol, 2007, 65: 12–20

    Google Scholar 

  9. Yang Y, Xu M, Guo J, et al. Bacterial extracellular electron transfer in bioelectrochemical systems. Process Biochem, 2012, 47: 1707–1714

    Google Scholar 

  10. Kumar R, Singh L, Zularisam A W. Exoelectrogens: Recent advances in molecular drivers involved in extracellular electron transfer and strategies used to improve it for microbial fuel cell applications. Renew Sustain Energy Rev, 2016, 56: 1322–1336

    Google Scholar 

  11. Lovley D R. Live wires: Direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ Sci, 2011, 4: 4896

    Google Scholar 

  12. Malvankar N S, Lovley D R. Microbial nanowires for bioenergy applications. Curr Opin Biotech, 2014, 27: 88–95

    Google Scholar 

  13. Malvankar N S, Tuominen M T, Lovley D R. Biofilm conductivity is a decisive variable for high-current-density Geobacter sulfurreducens microbial fuel cells. Energy Environ Sci, 2012, 5: 5790

    Google Scholar 

  14. Michelson K, Sanford R A, Valocchi A J, et al. Nanowires of Geobacter sulfurreducens require redox cofactors to reduce metals in pore spaces too small for cell passage. Environ Sci Tech, 2017, 51: 11660–11668

    Google Scholar 

  15. Logan B E. Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Micro, 2009, 7: 375–381

    Google Scholar 

  16. Bond D R, Lovley D R. Electricity production by geobacter sulfurreducens attached to electrodes. Appl Environ MicroBiol, 2003, 69: 1548–1555

    Google Scholar 

  17. Ringeisen B R, Ray R, Little B. A miniature microbial fuel cell operating with an aerobic anode chamber. J Power Sources, 2007, 165: 591–597

    Google Scholar 

  18. Pant D, Van Bogaert G, Diels L, et al. A review of the substrates used in microbial fuel cells (MFCs) for sustainable energy production. Bioresource Tech, 2010, 101: 1533–1543

    Google Scholar 

  19. Pandey P, Shinde V N, Deopurkar R L, et al. Recent advances in the use of different substrates in microbial fuel cells toward wastewater treatment and simultaneous energy recovery. Appl Energy, 2016, 168: 706–723

    Google Scholar 

  20. Kim J R, Jung S H, Regan J M, et al. Electricity generation and microbial community analysis of alcohol powered microbial fuel cells. Bioresource Tech, 2007, 98: 2568–2577

    Google Scholar 

  21. Choi J, Chang H N, Han J I. Performance of microbial fuel cell with volatile fatty acids from food wastes. Biotechnol Lett, 2011, 33: 705–714

    Google Scholar 

  22. Jung S, Regan J M. Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors. Appl Microbiol Biotechnol, 2007, 77: 393–402

    Google Scholar 

  23. Lee H S, Parameswaran P, Kato-Marcus A, et al. Evaluation of energy-conversion efficiencies in microbial fuel cells (MFCs) utilizing fermentable and non-fermentable substrates. Water Res, 2008, 42: 1501–1510

    Google Scholar 

  24. Chae K J, Choi M J, Lee J W, et al. Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Bioresource Tech, 2009, 100: 3518–3525

    Google Scholar 

  25. Yu J, Park Y, Kim B, et al. Power densities and microbial communities of brewery wastewater-fed microbial fuel cells according to the initial substrates. Bioprocess Biosyst Eng, 2015, 38: 85–92

    Google Scholar 

  26. Kiely P D, Rader G, Regan J M, et al. Long-term cathode performance and the microbial communities that develop in microbial fuel cells fed different fermentation endproducts. Bioresource Tech, 2011, 102: 361–366

    Google Scholar 

  27. Yang N, Hafez H, Nakhla G. Impact of volatile fatty acids on microbial electrolysis cell performance. Bioresource Tech, 2015, 193: 449–455

    Google Scholar 

  28. Mateo S, Cañizares P, Rodrigo M A, et al. Driving force behind electrochemical performance of microbial fuel cells fed with different substrates. Chemosphere, 2018, 207: 313–319

    Google Scholar 

  29. Zhang Y, Min B, Huang L, et al. Electricity generation and microbial community response to substrate changes in microbial fuel cell. Bioresource Tech, 2011, 102: 1166–1173

    Google Scholar 

  30. Ren Z, Ward T E, Regan J M. Electricity production from cellulose in a microbial fuel cell using a defined binary culture. Environ Sci Technol, 2007, 41: 4781–4786

    Google Scholar 

  31. Cheng S, Kiely P, Logan B E. Pre-acclimation of a wastewater inoculum to cellulose in an aqueous-cathode MEC improves power generation in air-cathode MFCs. Bioresource Tech, 2011, 102: 367–371

    Google Scholar 

  32. Rezaei F, Xing D, Wagner R, et al. Simultaneous cellulose degradation and electricity production by enterobacter cloacae in a microbial fuel cell. Appl Environ MicroBiol, 2009, 75: 3673–3678

    Google Scholar 

  33. 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

    Google Scholar 

  34. Ishii S, Suzuki S, Norden-Krichmar T M, et al. Microbial population and functional dynamics associated with surface potential and carbon metabolism. ISME J, 2014, 8: 963–978

    Google Scholar 

  35. Freguia S, Teh E H, Boon N, et al. Microbial fuel cells operating on mixed fatty acids. Bioresource Tech, 2010, 101: 1233–1238

    Google Scholar 

  36. Liu H, Cheng S, Logan B E. Production of electricity from acetate or butyrate using a single-chamber microbial fuel cell. Environ Sci Technol, 2005, 39: 658–662

    Google Scholar 

  37. Jang J K, Chang I S, Hwang H Y, et al. Electricity generation coupled to oxidation of propionate in a microbial fuel cell. Biotechnol Lett, 2010, 32: 79–85

    Google Scholar 

  38. de Cárcer D A, Ha P T, Jang J K, et al. Microbial community differences between propionate-fed microbial fuel cell systems under open and closed circuit conditions. Appl Microbiol Biotechnol, 2011, 89: 605–612

    Google Scholar 

  39. Sun Q, Li Z L, Wang Y Z, et al. Cathodic bacterial community structure applying the different co-substrates for reductive decolorization of Alizarin Yellow R. Bioresource Tech, 2016, 208: 64–72

    Google Scholar 

  40. Sun J, Hu Y Y, Bi Z, et al. Simultaneous decolorization of azo dye and bioelectricity generation using a microfiltration membrane air-cathode single-chamber microbial fuel cell. Bioresource Tech, 2009, 100: 3185–3192

    Google Scholar 

  41. Wang X, Feng Y, Wang H, et al. Bioaugmentation for electricity generation from corn stover biomass using microbial fuel cells. Environ Sci Technol, 2009, 43: 6088–6093

    Google Scholar 

  42. Lovley D R, Giovannoni S J, White D C, et al. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch Microbiol, 1993, 159: 336–344

    Google Scholar 

  43. Kiely P D, Regan J M, Logan B E. The electric picnic: Synergistic requirements for exoelectrogenic microbial communities. Curr Opin Biotech, 2011, 22: 378–385

    Google Scholar 

  44. Montpart N, Rago L, Baeza J A, et al. Hydrogen production in single chamber microbial electrolysis cells with different complex substrates. Water Res, 2015, 68: 601–615

    Google Scholar 

  45. Harnisch F, Koch C, Patil S A, et al. Revealing the electrochemically driven selection in natural community derived microbial biofilms using flow-cytometry. Energy Environ Sci, 2011, 4: 1265

    Google Scholar 

  46. Brown D G, Komlos J, Jaffé P R. Simultaneous utilization of acetate and hydrogen by Geobacter sulfurreducens and implications for use of hydrogen as an indicator of redox conditions. Environ Sci Technol, 2005, 39: 3069–3076

    Google Scholar 

  47. Flayac C, Trably E, Bernet N. Microbial anodic consortia fed with fermentable substrates in microbial electrolysis cells: Significance of microbial structures. Bioelectrochemistry, 2018, 123: 219–226

    Google Scholar 

  48. Ishii S, Suzuki S, Tenney A, et al. Comparative metatranscriptomics reveals extracellular electron transfer pathways conferring microbial adaptivity to surface redox potential changes. ISME J, 2018, 12: 2844–2863

    Google Scholar 

  49. Rosenbaum M A, Bar H Y, Beg Q K, et al. Shewanella oneidensis in a lactate-fed pure-culture and a glucose-fed co-culture with Lactococcus lactis with an electrode as electron acceptor. Bioresource Tech, 2011, 102: 2623–2628

    Google Scholar 

  50. Kim B. Dynamic effects of learning capabilities and profit structures on_the innovation competition. Optim Control Appl Meth, 1999, 20: 127–144

    Google Scholar 

  51. von Canstein H, Ogawa J, Shimizu S, et al. Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ MicroBiol, 2008, 74: 615–623

    Google Scholar 

  52. Milliken C E, May H D. Sustained generation of electricity by the spore-forming, Gram-positive, Desulfitobacterium hafniense strain DCB2. Appl Microbiol Biotechnol, 2007, 73: 1180–1189

    Google Scholar 

  53. Kiely P D, Call D F, Yates M D, et al. Anodic biofilms in microbial fuel cells harbor low numbers of higher-power-producing bacteria than abundant genera. Appl Microbiol Biotechnol, 2010, 88: 371–380

    Google Scholar 

  54. Zhao Y G, Zhang Y, She Z, et al. Effect of substrate conversion on performance of microbial fuel cells and anodic microbial communities. Environ Eng Sci, 2017, 34: 666–674

    Google Scholar 

  55. Müller N, Worm P, Schink B, et al. Syntrophic butyrate and propionate oxidation processes: From genomes to reaction mechanisms. Environ MicroBiol Rep, 2010, 2: 489–499

    Google Scholar 

  56. Liu X, Zhuo S, Rensing C, et al. Syntrophic growth with direct interspecies electron transfer between pili-free Geobacter species. ISME J, 2018, 12: 2142–2151

    Google Scholar 

  57. Bond D R, Holmes D E, Tender L M, et al. Electrode-reducing microorganisms that harvest energy from marine sediments. Science, 2002, 295: 483–485

    Google Scholar 

  58. Vandižurová A, Bódy G, Javorský P, et al. Actinomyces ruminicola G10—The rumen bacterium recovered from glycerol enriched cultivation media. Nova BioTech Chim, 2013, 12: 39–45

    Google Scholar 

  59. Pham T H, Boon N, Aelterman P, et al. Metabolites produced by Pseudomonas sp. enable a Gram-positive bacterium to achieve extracellular electron transfer. Appl Microbiol Biotechnol, 2008, 77: 1119–1129

    Google Scholar 

  60. Bosire E M, Blank L M, Rosenbaum M A. Strain- and substrate-dependent redox mediator and electricity production by Pseudomonas aeruginosa. Appl Environ Microbiol, 2016, 82: 5026–5038

    Google Scholar 

  61. He Z, Minteer S D, Angenent L T. Electricity generation from artificial wastewater using an upflow microbial fuel cell. Environ Sci Technol, 2005, 39: 5262–5267

    Google Scholar 

  62. Freguia S, Rabaey K, Yuan Z, et al. Syntrophic processes drive the conversion of glucose in microbial fuel cell anodes. Environ Sci Technol, 2008, 42: 7937–7943

    Google Scholar 

  63. Parameswaran P, Torres C I, Lee H S, et al. Syntrophic interactions among anode respiring bacteria (ARB) and Non-ARB in a biofilm anode: Electron balances. Biotechnol Bioeng, 2009, 103: 513–523

    Google Scholar 

  64. Parameswaran P, Zhang H, Torres C I, et al. Microbial community structure in a biofilm anode fed with a fermentable substrate: The significance of hydrogen scavengers. Biotechnol Bioeng, 2010, 105: 69–78

    Google Scholar 

  65. Kaur A, Boghani H C, Michie I, et al. Inhibition of methane production in microbial fuel cells: Operating strategies which select electrogens over methanogens. Bioresource Tech, 2014, 173: 75–81

    Google Scholar 

  66. Mahmoud M, Torres C I, Rittmann B E. Changes in glucose fermentation pathways as a response to the free ammonia concentration in microbial electrolysis cells. Environ Sci Tech, 2017, 51: 13461–13470

    Google Scholar 

  67. Morris J M, Jin S. Influence of NO3 and SO4 on power generation from microbial fuel cells. Chem Eng J, 2009, 153: 127–130

    Google Scholar 

  68. Su S G, Cheng H Y, Zhu T T, et al. Kinetic competition between microbial anode respiration and nitrate respiration in a bioelectrochemical system. Bioelectrochemistry, 2018, 123: 241–247

    Google Scholar 

  69. Liu Y, Ding M, Ling W, et al. A three-species microbial consortium for power generation. Energy Environ Sci, 2017, 10: 1600–1609

    Google Scholar 

  70. Kim C, Song Y E, Lee C R, et al. Glycerol-fed microbial fuel cell with a co-culture of Shewanella oneidensis MR-1 and Klebsiella pneumonae J2B. J Ind Microbiol Biotechnol, 2016, 43: 1397–1403

    Google Scholar 

  71. Venkataraman A, Rosenbaum M A, Perkins S D, et al. Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems. Energy Environ Sci, 2011, 4: 4550

    Google Scholar 

  72. Schmitz S, Rosenbaum M A. Boosting mediated electron transfer in bioelectrochemical systems with tailored defined microbial cocultures. Biotech Bioeng, 2018, 13

  73. Zhou M, Freguia S, Dennis P G, et al. Development of bioelectrocatalytic activity stimulates mixed-culture reduction of glycerol in a bioelectrochemical system. Microbial Biotech, 2015, 8: 483–489

    Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant Nos. 21876090, 21577068), the Tianjin Research Program of Application Foundation and Advanced Technology (Grant No. 18JCZDJC39400), the Fundamental Research Funds for the Central Universities (Grant No. C029188008), and the 111 Program of the Ministry of Education of China (Grant No. T2017002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xin Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yan, Y., Wang, X. Ecological responses to substrates in electroactive biofilm: A review. Sci. China Technol. Sci. 62, 1657–1669 (2019). https://doi.org/10.1007/s11431-018-9410-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11431-018-9410-6

En

Navigation