Skip to main content
SpringerLink
Log in

Extracellular electron transfer modes and rate-limiting steps in denitrifying biocathodes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Denitrifying bioelectrochemical system provided an alternative technology for nitrogen removal, even power recovery from wastewater, and its nitrogen removal performance and intermediate accumulation were affected by the extracellular electron transfer modes and rate-limiting steps in denitrifying biocathodes. In the current study, the extracellular electron transfer modes and rate-limiting steps for nitrate reduction and nitrite reduction of denitrifying biocathode were investigated through cyclic voltammetry. When the cathode potential swept from 0.003 to − 0.897 V (vs. Ag/AgCl), denitrifiers were indispensable for electrochemical denitrification. Three peak potentials were found in the cyclic voltammogram of denitrifying biocathode, where E1 (− 0.471 to − 0.465 V) and E2 (− 0.412 to − 0.428 V) represented respectively nitrate reduction and nitrite oxidation while E3 (− 0.822 to − 0.826 V) represented nitrite reduction. Nitrate reduction involved the direct electron transfer mode while nitrite reduction involved the mediated electron transfer mode. Intracellular catalytic reaction was the rate-limiting step for nitrate reduction, independent on the electrochemical activity of denitrifying biocathode and the nitrate supply. The nitrate supply posed an effect on the rate-limiting step for nitrite reduction. The mediator transfer was the rate-limiting step for nitrite reduction in the absence of nitrate. But both mediator transfer and intracellular catalytic reaction became the rate-limiting steps for nitrite reduction in the presence of sufficient nitrate.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • APHA (2012) Standard methods for the examination of water and wastewater. American Public Health Association, Washington DC

    Google Scholar 

  • Ashok V, Hait S (2015) Remediation of nitrate-contaminated water by solid-phase denitrification process-a review. Environ Sci Pollut Res 22:8075–8093

    Article  CAS  Google Scholar 

  • Bajracharya S, Sharma M, Mohanakrishna G, Benneton XD, Strik DPBTB, Sarma PM, Pant D (2016) An overview on emerging bioelectrochemical systems (BESs): technology for sustainable electricity, waste remediation, resource recovery, chemical production and beyond. Renew Energy 98:153–170

    Article  CAS  Google Scholar 

  • Bard AJ, Faulkner LR (2001) Electrochemical methods: fundamentals and applications. Wiley, New York

    Google Scholar 

  • Chen J, Strous M (2013) Denitrification and aerobic respiration, hybrid electron transport chains and co-evolution. Bba-bioenergetics 1827:136–144

    Article  CAS  Google Scholar 

  • Chen GW, Choi SJ, Cha JH, Lee TH, Kim CW (2010) Microbial community dynamics and electron transfer of a biocathode in microbial fuel cells. Korean J Chem Eng 27:1513–1520

    Article  CAS  Google Scholar 

  • Clauwaert P, Rabaey K, Aelterman P, De Schamphelaire L, Ham TH, Boeckx P, Boon N, Verstraete W (2007) Biological denitrification in microbial fuel cells. Environ Sci Technol 41:3354–3360

    Article  CAS  Google Scholar 

  • Ding A, Zhao D, Ding F, Du S, Lu H, Zhang M, Zheng P (2018) Effect of inocula on performance of bio-cathode denitrification and its microbial mechanism. Chem Eng J 343:399–407

    Article  CAS  Google Scholar 

  • Finkelstein DA, Tender LM, Zeikus JG (2006) Effect of electrode potential on electrode-reducing microbiota. Environ Sci Technol 40:6990–6995

    Article  CAS  Google Scholar 

  • Freguia S, Masuda M, Tsujimura S, Kano K (2009) Lactococcus lactis catalyses electricity generation at microbial fuel cell anodes via excretion of a soluble quinone. Bioelectrochemistry 76:14–18

    Article  CAS  Google Scholar 

  • Freguia S, Tsujimura S, Kano K (2010) Electron transfer pathways in microbial oxygen biocathodes. Electrochim Acta 55:813–818

    Article  CAS  Google Scholar 

  • Fricke K, Harnisch F, Schröder U (2008) On the use of cyclic voltammetry for the study of anodic electron transfer in microbial fuel cells. Energy Environ Sci 1:144–147

    Article  CAS  Google Scholar 

  • Harnisch F, Freguia S (2012) A basic tutorial on cyclic voltammetry for the investigation of electroactive microbial biofilms. Chem-asian J 7:466–475

    Article  CAS  Google Scholar 

  • Jiang C, Yang Q, Wang D, Zhong Y, Chen F, Li X, Zeng G, Li X, Shang M (2017) Simultaneous perchlorate and nitrate removal coupled with electricity generation in autotrophic denitrifying biocathode microbial fuel cell. Chem Eng J 308:783–790

    Article  CAS  Google Scholar 

  • Karimi-Maleh H, Moazampour M, Ensafi AA, Mallakpour S, Hatami M (2014) An electrochemical nanocomposite modified carbon paste electrode as a sensor for simultaneous determination of hydrazine and phenol in water and wastewater samples. Environ Sci Pollut Res 21:5879–5888

    Article  CAS  Google Scholar 

  • Khater DZ, El-Khatib KM, Hassan RYA (2018) Exploring the bioelectrochemical characteristics of activated sludge using cyclic voltammetry. Appl Biochem Biotechnol 184:92–101

    Article  CAS  Google Scholar 

  • Kondaveeti S, Min B (2013) Nitrate reduction with biotic and abiotic cathodes at various cell voltages in bioelectrochemical denitrification system. Bioprocess Biosyst Eng 36:231–238

    Article  CAS  Google Scholar 

  • Light SH, Su L, Rivera-Lugo R, Cornejo JA, Louie A, Iavarone AT, Ajo-Franklin CM, Portnoy DA (2018) A flavin-based extracellular electron transfer mechanism in diverse gram-positive bacteria. Nature 562:140–144

    Article  CAS  Google Scholar 

  • Nguyen VK, Hong S, Park Y, Jo K, Lee T (2015) Autotrophic denitrification performance and bacterial community at biocathodes of bioelectrochemical systems with either abiotic or biotic anodes. J Biosci Bioeng 119:180–187

    Article  CAS  Google Scholar 

  • Pandey P, Shinde VN, Deopurkar RL, Kale SP, Patil SA, Pant D (2016) Recent advances in the use of different substrates in microbial fuel cells toward wastewater treatment and simultaneous energy recovery. Appl Energy 168:706–723

    Article  CAS  Google Scholar 

  • Pous N, Koch C, Colprim J, Puig S, Harnisch F (2014) Extracellular electron transfer of biocathodes: revealing the potentials for nitrate and nitrite reduction of denitrifying microbiomes dominated by Thiobacillus sp. Electrochem Commun 49:93–97

    Article  CAS  Google Scholar 

  • Pous N, Puig S, Dolors Balaguer M, Colprim J (2015) Cathode potential and anode electron donor evaluation for a suitable treatment of nitrate-contaminated groundwater in bioelectrochemical systems. Chem Eng J 263:151–159

    Article  CAS  Google Scholar 

  • Rabaey K, Rozendal RA (2010) Microbial electrosynthesis - revisiting the electrical route for microbial production. Nat Rev Microbiol 8:706–716

    Article  CAS  Google Scholar 

  • Sathishkumar K, Narenkumar J, Selvi A, Murugan K, Babujanarthanam R, Rajasekar A (2018) Treatment of soak liquor and bioelectricity generation in dual chamber microbial fuel cell. Environ Sci Pollut Res 25:11424–11430

    Article  CAS  Google Scholar 

  • Sun H, Xu S, Zhuang G, Zhuang X (2016) Performance and recent improvement in microbial fuel cells for simultaneous carbon and nitrogen removal: a review. J Environ Sci China 39:242–248

    Article  Google Scholar 

  • Vilarsanz A, Pous N, Puig S, Balaguer MD, Colprim J, Bañeras L (2018) Denitrifying nirK-containing alphaproteobacteria exhibit different electrode driven nitrite reduction capacities. Bioelectrochemistry 121:74–83

    Article  CAS  Google Scholar 

  • Wang D, Wang Y, Liu Y, Ngo HH, Lian Y, Zhao J, Chen F, Yang Q, Zeng G, Li X (2017) Is denitrifying anaerobic methane oxidation-centered technologies a solution for the sustainable operation of wastewater treatment plants? Bioresour Technol 234:456–465

    Article  CAS  Google Scholar 

  • Wu Y, Wang D, Liu X, Xu Q, Chen Y, Yang Q, Li H, Ni B (2019) Effect of poly aluminum chloride on dark fermentative hydrogen accumulation from waste activated sludge. Water Res 153:217–228

    Article  CAS  Google Scholar 

  • Xiao Z, Awata T, Zhang D, Zhang C, Li Z, Katayama A (2016) Enhanced denitrification of Pseudomonas stutzeri by a bioelectrochemical system assisted with solid-phase humin. J Biosci Bioeng 122:85–91

    Article  CAS  Google Scholar 

  • Xu Q, Liu X, Wang D, Wu Y, Wang Q, Liu Y, Li X, An H, Zhao J, Chen F, Zhong Y, Yang Q, Zeng G (2018) Free ammonia-based pretreatment enhances phosphorus release and recovery from waste activated sludge. Chemosphere 213:276–284

    Article  CAS  Google Scholar 

  • Yang G, Huang L, You L, Zhuang L, Zhou S (2017) Electrochemical and spectroscopic insights into the mechanisms of bidirectional microbe-electrode electron transfer in Geobacter soli biofilms. Electrochem Commun 77:93–97

    Article  CAS  Google Scholar 

  • Yu L, Yuan Y, Chen S, Zhuang L, Zhou S (2015) Direct uptake of electrode electrons for autotrophic denitrification by Thiobacillus denitrificans. Electrochem Commun 60:126–130

    Article  CAS  Google Scholar 

  • Zeng XF, Borole AP, Pavlostathis SG (2018) Processes and electron flow in a microbial electrolysis cell bioanode fed with furanic and phenolic compounds. Environ Sci Pollut Res 25:35981–35989

    Article  CAS  Google Scholar 

  • Zhang G, Zhang H, Zhang C, Zhang G, Yang F, Yuan G, Gao F (2013) Simultaneous nitrogen and carbon removal in a single chamber microbial fuel cell with a rotating biocathode. Process Biochem 48:893–900

    Article  CAS  Google Scholar 

  • Zhang S, Bao R, Lu J, Sang W (2018) Simultaneous sulfide removal, nitrification, denitrification and electricity generation in three-chamber microbial fuel cells. Sep Purif Technol 195:314–321

    Article  CAS  Google Scholar 

  • Zhong L, Zhang S, Wei Y, Bao R (2017) Power recovery coupled with sulfide and nitrate removal in separate chambers using a microbial fuel cell. Biochem Eng J 124:6–12

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 21577108).

Author information

Authors and Affiliations

  1. School of Civil Engineering and Architecture, Wuhan University of Technology, Wuhan, 430070, China

    Ke Wang & Shaohui Zhang

Authors
  1. Ke Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaohui Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Shaohui Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Bingcai Pan

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, K., Zhang, S. Extracellular electron transfer modes and rate-limiting steps in denitrifying biocathodes. Environ Sci Pollut Res 26, 16378–16387 (2019). https://doi.org/10.1007/s11356-019-05117-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05117-x

Keywords

Search

Navigation