Abstract
Both anode potentials and substrates can affect the process of biofilm formation in bioelectrochemical systems, but it is unclear who primarily determine the anode-respiring bacteria (ARB) community structure and composition. To address this issue, we divided microbial electrolysis cells (MECs) into groups, feeding them with different substrates and culturing them at various potentials. Non-turnover cyclic voltammetry indicated that the extracellular electron transfer components were uniform when feeding acetate, because the same oxidation peaks occurred at − 0.36 ± 0.01 and − 0.17 ± 0.01 V (vs. Ag/AgCl). Illumina MiSeq sequencing revealed that the dominating ARB was Geobacter, which did not change with different potentials. When the MECs were cultured with sucrose and mixed substrates, oxidation peak P3 (− 0.29 ± 0.015 V) occurred at potentials of − 0.29 and 0.01 V. This may be because of the appearance of Unclassified_AKYG597. In addition, oxidation peak P4 (− 0.99 ± 0.01 V) occurred at high and low potentials (0.61 and − 0.45 V, respectively), and the maximum current densities were far below those of the middle potentials. Illumina MiSeq sequencing showed that fermentation microorganisms (Lactococcus and Sphaerochaeta) dominated the biofilms. Consequently, substrate primarily determined the dominating ARB, and Geobacter invariably dominated the acetate-fed biofilms with potentials changed. Conversely, different potentials mainly affected fermentable substrate-fed biofilms, with dominating ARB turning into Unclassified_AKYG59.
Similar content being viewed by others
References
Box JB (1983) Investigation of the Folin-Ciocalteau phenol reagent for the determination of polyphenolic substances in natural waters. Water Res 17:511–525
Call D, Logan BE (2008) Hydrogen production in a single chamber microbial electrolysis cell lacking a membrane. Environ Sci Technol 42:3401–3406
Cao XX, Huang X, Liang P, Xiao K, Zhou YJ, Zhang XY, Logan BE (2009) A new method for water desalination using microbial desalination cells. Environ Sci Technol 43:7148–7152
Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. PNAS 108:4516–4522
Capozzi V, Fiocco D, Amodio ML, Gallone A, Spano G (2009) Bacterial stressors in minimally processed food. Int J Mol Sci 10:3076–3105
Chae KJ, Choi MJ, Lee JW, Kim KY, Kim IS (2009) Effect of different substrates on the performance, bacterial diversity, and bacterial viability in microbial fuel cells. Bioresour Technol 100:3518–3525
Cheng KY, Ho G, Cordruwisch R (2008) Affinity of microbial fuel cell biofilm for the anodic potential. Environ Sci Technol 42:3828–3834
Commault AS, Lear G, Weld RJ (2015) Maintenance of Geobacter-dominated biofilms in microbial fuel cells treating synthetic wastewater. Bioelectrochemistry 106:150–158
Finkelstein DA, Tender LM, Zeikus JG (2006) Effect of electrode potential on electrode-reducing microbiota. Environ Sci Technol 40:6990–6995
Freguia S (2009) Lactococcus lactis catalyses electricity generation at microbial fuel cell anodes via excretion of a soluble quinone. Bioelectrochemistry 76:14–18
Inoue K, Qian XL, Morgado L, Kim BC, Mester T, Izallalen M, Salgueiro CA, Lovley DR (2010) Purification and characterization of OmcZ, an outer-surface, octaheme c-type cytochrome essential for optimal current production by Geobacter sulfurreducens. Appl Environ Microbiol 76:3999–4007
Jung S, Regan JM (2007) Comparison of anode bacterial communities and performance in microbial fuel cells with different electron donors. Appl Microbiol Biotechnol 77:393–402
Kiely PD, Cusick R, Call DF, Selembo PA, Regan JM, Logan BE (2011) Anode microbial communities produced by changing from microbial fuel cell to microbial electrolysis cell operation using two different wastewaters. Bioresour Technol 102:388–394
Kumar A, Siggins A, Katuri K, Mahony T, O’Flaherty V, Lens P, Leech D (2013) Catalytic response of microbial biofilms grown under fixed anode potentials depends on electrochemical cell configuration. Chem Eng J 230:532–536
Liu H, Ramnarayanan R, Logan BE (2004) Production of electricity during wastewater treatment using a single chamber microbial fuel cell. Environ Sci Technol 38:2281–2285
Logan BE (2009) Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Microbiol 7:375–381
Logan BE, Hamelers B, Rozendal RA, Schrorder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K (2006) Microbial fuel cells: methodology and technology. Environ Sci Technol 40:5181–5192
Marsili E, Sun J, Bond DR (2010) Voltammetry and growth physiology of Geobacter sulfurreducens biofilms as a function of growth stage and imposed electrode potential. Electroanalysis 22:865–874
Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Nevin KP, Richter H, Covalla SF, Johnson JP, Woodard TL, Orloff AL (2008) Power output and columbic efficiencies from biofilms of Geobacter sulfurreducens, comparable to mixed community microbial fuel cells. Environ Microbiol 10:2505–2514
Pant D, Singh A, Van Bogaert G, Olsen SI, Nigam PS, Diels L, Vanbroekhoven K (2012) Bioelectrochemical systems (BES) for sustainable energy production and product recovery from organic wastes and industrial wastewaters. RSC Adv 2:1248–1263
Park I, Kim BC (2011) Homologous overexpression of omcZ, a gene for an outer surface c-type cytochrome of Geobacter sulfurreducens by single-step gene replacement. Biotechnol Lett 33:2043–2048
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res 41:590–596
Sousa DZ, Pereira MA, Alves JI, Smidt H, Stams AJ, Alves MS (2008) Anaerobic microbial LCFA degradation in bioreactors. Water Sci Technol 57:439–444
Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM (2011) On the electrical conductivity of microbial nanowires and biofilms. Energy Environ Sci 4:4366–4379
Torres CI, Krajmalnik-Brown R, Parameswaran P, Marcus AK, Wanger G, Gorby YA, Rittmann BE (2009) Selecting anode-respiring bacteria based on anode potential: phylogenetic, electrochemical, and microscopic characterization. Environ Sci Technol 43:9519–9524
Torres CI, Marcus AK, Lee HS, Parameswaran P, Krajmalnik-Brown R, Rittmann BE (2010) A kinetic perspective on extracellular electron transfer by anode-respiring bacteria. FEMS Microbiol Rev 34:3–17
Wagner RC, Call DF, Logan BE (2010) Optimal set anode potentials vary in bioelectrochemical systems. Environ Sci Technol 44:6036–6041
Wang X, Feng YJ, Ren NQ, Wang HM, Lee H, Li N, Zhao QL (2009) Accelerated start-up of two-chambered microbial fuel cells: effect of anodic positive poised potential. Electrochim Acta 54:1109–1114
Wei JC, Liang P, Cao XX, Huang X (2010) A new insight into potential regulation on growth and power generation of Geobacter sulfurreducens in microbial fuel cells based on energy viewpoint. Environ Sci Technol 44:3187–3191
Xing D, Cheng S, Regan JM, Logan BE (2009) Change in microbial communities in acetate- and glucose-fed microbial fuel cells in the presence of light. Biosens Bioelectron 25:105–111
Yates MD, Kiely PD, Call DF, Risman-Yazdi H, Bibby K, Peccia J, Regan JM, Logan BE (2012) Convergent development of anodic bacterial communities in microbial fuel cells. ISME J 6:2002–2013
Zhu XP, Yates MD, Logan BE (2012) Set potential regulation reveals additional oxidation peaks of Geobacter sulfurreducens anodic biofilms. Electrochem Commun 22:116–119
Zhu XP, Yates MD, Hatzell MC, Anand RH, Saikaly PE, Logan BE (2013) Microbial community composition is unaffected by anode potential. Environ Sci Technol 48:1352–1358
Funding
This research was supported by the National Natural Science Foundation of China (grant number 51478431), the Science and Technology Planning Project from the Science and Technology Department in Zhejiang Province (grant number LQ17E080002), the Innovative and Entrepreneurial Training Plan of National College Students (grant number GJ201623003), and the Xinmiao Talent Project in Zhejiang province (grant numbers 2016R408030, 2016R408028).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
This paper does not contain studies with human participants or animals performed by any of the authors.
Conflict of interest
The authors declare that they have no competing interests.
Electronic supplementary material
ESM 1
(PDF 1332 kb)
Rights and permissions
About this article
Cite this article
Ying, X., Guo, K., Chen, W. et al. The impact of electron donors and anode potentials on the anode-respiring bacteria community. Appl Microbiol Biotechnol 101, 7997–8005 (2017). https://doi.org/10.1007/s00253-017-8518-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-017-8518-8