Bacterial community shift and improved performance induced by in situ preparing dual graphene modified bioelectrode in microbial fuel cell

doi:10.1016/j.biortech.2017.04.044

Bioresource Technology

Volume 238, August 2017, Pages 273-280

https://doi.org/10.1016/j.biortech.2017.04.044 Get rights and content

Highlights

•
D-GM-BE was prepared by microbial-induced reduction of GO and polarity reversion.
•
Proteobacteria and Firmicutes were the dominant bacteria in GM-BE.
•
Typical exoelectrogens in GM-BE shared much higher proportion.
•
The maximum power density obtained by D-GM-BE MFC was 2.34 times than C-BE-MFC.

Abstract

Dual graphene modified bioelectrode (D-GM-BE) was prepared by in situ microbial-induced reduction of graphene oxide (GO) and polarity reversion in microbial fuel cell (MFC). Next Generation Sequencing technology was used to elucidate bacterial community shift in response to improved performance in D-GM-BE MFC. The results indicated an increase in the relative ratio of Proteobacteria, but a decrease of Firmicutes was observed in graphene modified bioanode (GM-BA); increase of Proteobacteria and Firmicutes were observed in graphene modified biocathode (GM-BC). Genus analysis demonstrated that GM-BE was beneficial to enrich electrogens. Typical exoelectrogens were accounted for 13.02% and 8.83% in GM-BA and GM-BC. Morphology showed that both GM-BA and GM-BC formed 3D-like graphene/biofilm architectures and revealed that the biofilm viability and thickness would decrease to some extent when GM-BE was formed. D-GM-BE MFC obtained the maximum power density by 124.58 ± 6.32 mW m⁻², which was 2.34 times over C-BE MFC.

Graphical abstract

Introduction

Bacteria is regarded as catalysts to convert chemical energy into electricity in microbial fuel cell (MFC), which plays a huge role in the processes of extracellular electron transfer (EET) and energy transfer (Logan and Regan, 2006, Zhao et al., 2017). Obtaining the microbial structure and community in bioelectrode MFC is one of the significant elements to improve the MFC performance, which is beneficial for the development and application of MFC (Xu et al., 2017).

With the development of metagenomics, the Next Generation Sequencing technology has been applied to characterize microbial communities in MFCs in recent studies (Daghio et al., 2015). Luo et al. (2016) discussed the microbial communities in anode biofilm with high concentration of sodium acetate, which indicated that Proteobacteria, Bacteroidetes, and Synergistetes were the dominant phylum, and identified Geobacter as the dominant genus. To explain the high performance of aerobic biocathode MFC, Milner et al. (2016) studied the microbial community of aerobic biocathode with high oxygen reduction reaction (ORR) activity, which demonstrated that uncultured Gammaproteobacteria dominated the high performance and high ORR activity of aerobic biocathode MFC. These studies stated that metagenomics has been served in the field of MFC successfully, and metagenomics would provide much more microbial information to drive the development of MFC.

Graphene is a promising material with excellent physical/chemical characteristics (Cai et al., 2016), which has been applied in MFCs via different modes. In MFCs, graphene modifying anode is generally realized by coating graphene on electrode (Mehdinia et al., 2014), electrodepositing polymer on graphene nanosheets (Shaari and Kamarudin, 2017), etc.; graphene modifying cathode is usually completed by doping N (Hou et al., 2016), Fe (Tang et al., 2017) or Mn (Khilari et al., 2013) to graphene on electrode. These modifying methods are relative complicated and a large amount of chemicals are required. However, there existed an interesting phenomenon: graphene oxide (GO) could be in situ reduced by Shewanella (Wang et al., 2011), Escherichia coli (Gurunathan et al., 2013), etc., which were significant composition of exoelectrogens in MFCs. Owing to its easy operation and environmental friendliness, this approach has been developed in MFCs. Yong et al. (2014) fabricated 3D macroporous rGO/bacteria hybrid biofilm in MFC anode by self-assembly of GO via Shewanella oneidensis MR-1, which improved power density and EET process. Yuan et al. (2012) constructed graphene scaffolds anode by in situ microbially reduced GO via mixed bacteria, which increased power density and coulombic efficiency (CE) in MFCs. This method was relatively easy to be achieved in MFC anode, but there existed development space for in situ modifying cathode. Zhuang et al. (2012) implanted the microbially reduced graphene (completed in anode) into cathode, which formed 3D graphene/biofilm biocathode and enhanced catalytic activity to oxygen reduction reaction (ORR). In our previous studies, in situ graphene modified biocathode (GM-BC) was built by microbial-induced reduction of GO in anode and conducting polarity reversion to graphene modified bioanode (GM-BA), which proved to be an effective method to in situ prepare GM-BC. Based on in situ microbial-induced reduction of GO and polarity reversion, a three-step method to prepare in situ dual graphene modified bioelectrode (D-GM-BE) in a MFC was proposed: GM-BA was initially prepared via microbial-induced reduction of GO in anode; then GM-BC was prepared based on the polarity reversion of GM-BA; GM-BA was needed to be prepared once again.

In situ D-GM-BE is an important development direction for electrode modification. Whereas bacteria act the key role in the process of microbial-induced reduction and polarity reversion, therefore, it is necessary to master the inner regularity between graphene and bacteria. And this is quite critical to understand the complexity and assembly rule of in situ GM-BE, therefore, it is extremely urgent to study the bacterial community shift induced by in situ preparing D-GM-BE in MFC.

In this study, Next Generation Sequencing technology was used to investigate the bacterial community shift in response to in situ microbial-induced reduction and polarity reversion in D-GM-BE MFC. Understanding bioinformatics was of great significance for mastering mechanisms of EET process and ORR in D-GM-BE. Electrochemical analysis was performed to assess the performance of D-GM-BE MFC. Field emission scanning electron microscopy (FESEM) and confocal scanning laser microscopy (CSLM) were conducted to observe the changes of bacterial biofilms caused by in situ preparing D-GM-BE. This study aimed to provide bacterial information induced by in situ preparing D-GM-BE, and contribute to the development and application of D-GM-BE MFC.

Section snippets

MFC running conditions

A two-chamber MFC was adopted in this study, the volume of each chamber was 240 mL. Each MFC reactor was equipped with carbon felt (6 cm × 5 cm) as basic electrode. Anode and cathode chamber were separated by a cation exchange membrane (CEM) as our previous studies (Li et al., 2014, Sun et al., 2015), and active sludge was originally acquired from an urban sewage treatment plant in Guangzhou City. GO solution was synthesized by improved Hummers method (Chen et al., 2015), and GO solution (1 mg L⁻¹)

General characteristics of the pyrosequencing data

For the four biosamples, a total number of 207,774 valid sequences were achieved after quality control. The clean sequences for GM-BA, GM-BC, C-BA and C-BC were 51,387, 55,013, 48,774 and 52,600, respectively. The length of these valid sequences was principally about 100–220 bp, accounting for ∼99% of the total valid sequences. The mean length of these valid sequences was nearly 150 bp. The rarefaction curves of pyrosequencing based on V3 of 16S rRNA gene at genetic distance of 3% showed that

Conclusions

This study summarized bacterial community shift by Next Generation Sequencing technology in D-GM-BE MFC. Proteobacteria and Firmicutes were dominant bacteria in GM-BE in phylum level, and GM-BE was beneficial to enrich exoelectrogens. Typical exoelectrogens in GM-BE shared much higher proportion than those in C-BE. Morphology observation demonstrated that GM-BE formed 3D-like graphene/biofilm architectures. Owing to the enrichment of exoelectrogens, excellent electrochemical behavior of

Acknowledgements

The authors gratefully thank the financial support provided by the National Natural Science Fund of China (NO. 21477039, NO. U1401235 and NO. 51108186), Science and Technology Planning Project of Guangdong province, China (2014A020216042), Scientific and Technological Planning Project of Guangzhou, China (201607010318).

References (50)

W. Cai et al.
Enhanced hydrogen production in microbial electrolysis cell with 3D self-assembly nickel foam-graphene cathode
Biosens. Bioelectron.
(2016)
J. Chen et al.
Antibacterial activity of graphene-modified anode on Shewanella oneidensis MR-1 biofilm in microbial fuel cell
J. Power Sources
(2015)
J. Chen et al.
Intensive removal efficiency and mechanisms of carbon and ammonium in municipal wastewater treatment plant tail water by ozone oyster shells fix-bed bioreactor – membrane bioreactor combined system
Ecol. Eng.
(2017)
Y. Chen et al.
A review: driving factors and regulation strategies of microbial community structure and dynamics in wastewater treatment systems
Chemosphere
(2017)
M. Daghio et al.
Anodic and cathodic microbial communities in single chamber microbial fuel cells
New. Biotechnol.
(2015)
S. Gurunathan et al.
Microbial reduction of graphene oxide by Escherichia coli: a green chemistry approach
Colloids. Surf. B
(2013)
Y. Hou et al.
Nitrogen-doped graphene/CoNi alloy encased within bamboo-like carbon nanotube hybrids as cathode catalysts in microbial fuel cells
J. Power Sources
(2016)
F. Huang et al.
A fullerene colloidal suspension stimulates the growth and denitrification ability of wastewater treatment sludge-derived bacteria
Chemosphere
(2014)
K.-W. Jung et al.
Rapid formation of hydrogen-producing granules in an up-flow anaerobic sludge blanket reactor coupled with high-rate recirculation
Int. J. Hydrogen Energy
(2013)
R. Kumar et al.
Exoelectrogens: recent advances in molecular drivers involved in extracellular electron transfer and strategies used to improve it for microbial fuel cell applications
Renew. Sust. Energy Rev.
(2016)

Cited by (62)

Impact of bioelectricity on DNRA process and microbial community composition within cathodic biofilms in dual-chambered bioelectrode microbial fuel cell (MFC)
2024, Bioresource Technology
The synchronous bioelectricity generation and dissimilatory nitrate reduction to ammonium (DNRA) pathway in Klebsiella variicola C1 was investigated. The presence of bioelectricity facilitated cell growth on the anodic biofilms, consequently enhancing the nitrate removal efficiency decreasing total nitrogen levels and causing a negligible accumulation of NO₂^– in the supernatant. Genomic analysis revealed that K. variicola C1 possessed a complete DNRA pathway and largely annotated electron shuttles. The up-regulated expression of genes narG and nirB, encoding nitrite oxidoreductase and nitrite reductase respectively, was closely associated with increased extracellular electron transfer (EET). High-throughput sequencing analysis was employed to investigate the impact of bioelectricity on microbial community composition within cathodic biofilms. Results indicated that Halomonas, Marinobacter and Prolixibacteraceae were enriched at the cathode electrodes. In conclusion, the integration of a DNRA strain with MFC facilitated the efficient removal of wastewater containing high concentrations of NO₃^– and enabled the environmentally friendly recovery of NH₄⁺.
Crucial roles of microbial community and in-situ synthetic Bio-Ru<sup>0</sup> on diclofenac degradation and bioelectricity generation in a microbial fuel cell integrated electrocatalytic process
2024, Biochemical Engineering Journal
This study proposed methods of synthesizing Bio-Ru⁰ by microbial in-situ reduction and modified bio-anode to construct Bio-Ru⁰-anode-MFC for the diclofenac (DCF) degradation and bioelectricity generation performance. By analyzing XRD, XPS and observing SEM, TEM, Ru⁰ (Bio-Ru⁰) in-situ synthesized by anodic microorganisms, was distributed on surface of carbon felt electrode uniformly and formed reticular wire structure with cell secretion. Electrochemical tests demonstrated that the reticular structure promoted direct electron transfer between Bio-Ru⁰ and microorganisms. Under anaerobic conditions with sufficient carbon source, the DCF degradation efficiency of Bio-Ru⁰-anode MFC reached 67.20%, where Ru catalyzed reaction, microbial reaction, electrochemical reaction, and adsorption contributed to the DCF degradation by 34.32%, 30.20%, 21.67% and 13.81%, respectively. Benefitting from the synergistic effects of DCF-degrading bacteria, electroactive microorganisms, and Bio-Ru⁰ catalysis, DCF could achieve initially dechlorinated in Bio-Ru⁰-anode MFC, then completely converted to chlorine-free products after 2.68 d. Ru-tolerant bacteria such as Geobacter, Desulfovibrioceae, and Pseudomonas were enriched in bio-Ru⁰-anode and played a key role in DCF degradation. This study could provide new ideas for microbial in-situ synthesis of Bio-Ru⁰-anode to promote degradation of halogenated organic pollutants.
Magnetite-equipped algal-rich sediments for microbial fuel cells: Remediation of sediment organic matter pollution and mechanisms of remote electron transfer
2024, Science of the Total Environment
Using the bio-electrochemical methods for the restoration of high algae sediments is full of potential and challenges. How to promote extracellular electron transfer (EET) process in microbial fuel cells (MFC) is the key bottleneck. The study had explored the potential application of magnetite on accelerating electron transfer for improving the output of MFC and sediment pollution remediation. The results indicated that the organic matter degradation rate showed a remarkable increase of 27.45 %, and the voltage output was approximately 1.68 times higher compared to the MFC configured with regular sediment. Abundant electroactive bacteria (EABs), such as Geobacter and Burkholderiaceae, and fermentative bacteria were responsible for these results, accompanied by the enhanced fluorescence of humic substances (HS), increased concentration and activity of cytochrome C (25.05 % and 21.12 %), as well as elevated extracellular polymeric substance content. Moreover, the intrinsic EET mechanisms among Fe-oxides, HS, and EABs were explored. According to the electrochemical analysis and substance transformation, the EET process involved four stages: magnetite-enhanced direct electron transfer via strong conductivity, iron respiration mediating electron transfer to the electrode, the model quinone substance acting as an electron shuttle facilitating EET and iron reduction, and iron cycling mediating electron transfer. This study provides an effective strategy for pollution remediation in algal-rich sediment, which was beneficial for the harmless treatment and resource utilization of both algae and sediment, simultaneously.
Enhanced electrochemical performance by polyaniline (PANI) on covalent organic framework - Carbon nanotube (COF-CNT) as cathode catalyst for microbial fuel cells
2024, International Journal of Hydrogen Energy
Electrochemical catalysts based on polyaniline derived covalent organic framework-carbon nanotube composite (PANI@COF-CNT) was successfully fabricated by chemical oxidation polymerization method. Rougher surface morphologies of PANI@COF-CNT was obtained attributing to PANI loading with the porous framework, forming a unique well-distributed network structure. The specific surface area and pore diameter of PANI@COF-CNT were 99.533 m²/g and 24.916 nm, which were 13.220 and 1.913 times of that of PANI@COF. The output voltage of PANI@COF-CNT MFC could be stably sustained at about 0.390 V with no significant change after 120 h. The maximum power density of PANI@COF-CNT MFC was 194.480 mW/m², which was 8.655 folds higher than that of the pristine COF cathode MFC. The coral bone-like structure of COF and the porous structure of CNT provided abundant electroactive sites, and the high conductivity of PANI significantly enhanced the electron transfer rate and effectively reduced the transport resistance, which in turn effectively strengthened the electrochemical performance and cycling stability of MFC.
Fe-Ni alloy modified Zr-based MOF derivatives as bioelectrocatalyst for regulating multipath EET efficiency and biofilm electrogenic activity
2023, Applied Surface Science
As a green conversion device, the electricity performance of microbial fuel cell (MFC) was mainly affected by the extracellular electron transfer (EET) process of the biofilm. This paper presented the fabrication and characterization of carbonized derivatives composed with alloy nanoparticles (NPs) derived from Zr-based metal organic frameworks, which exhibited biocompatibility and high electrocatalytic activity. As the results of bioanodes, the charge transfer resistance decreased from 5.60 Ω (Zr-C) to 0.61 Ω (Fe/Ni-Zr-C), and the exchange current density increased from 0.56 mA/cm² (Zr-C) to 1.40 mA/cm² (Fe/Ni-Zr-C). Electrochemical tests and density functional theory (DFT) confirmed that Fe-Ni alloy NPs promoted the rapid transfer of electrons within the electrode and improved the EET efficiency mediated with the flavin compounds. High throughput sequencing and PICRUSt verified the specific screening function of Fe-Ni alloy for electrogenic bacteria (mainly Geoalkalibacter) and the promoting effect on the expression of flavin-related proteins in biofilm. The maximum power density of Fe/Ni-Zr-C MFC (5.09 W/m²) was higher than that of Ni-Zr-C (4.19 W/m²), Fe-Zr-C (3.58 W/m²) and Zr-C (3.09 W/m²) MFCs. Fe/Ni-Zr-C material can act as an economical and high-performance bioelectrocatalyst to improve the power generation capability of MFC by improving EET rate and energy conversion efficiency of biofilm.
Environmental biotechnology and the involving biological process using graphene-based biocompatible material
2023, Chemosphere
Biotechnology is a promising approach to environmental remediation but requires improvement in efficiency and convenience. The improvement of biotechnology has been illustrated with the help of biocompatible materials as biocarrier for environmental remediations. Recently, graphene-based materials (GBMs) have become promising materials in environmental biotechnology. To better illustrate the principle and mechanisms of GBM application in biotechnology, the comprehension of the biological response of microorganisms and enzymes when facing the GBMs is needed. The review illustrated distinct GBM-microbe/enzyme composites by providing the GBM-microbe/enzyme interaction and the determining factors. There are diverse GBM modifications for distinct biotechnology applications. Each of these methods and applications depends on the physicochemical properties of GBMs. The applications of these composites were mainly categorized as pollutant adsorption, anaerobic digestion, microbial fuel cells, and organics degradation. Where information was available, the strategies and mechanisms of GBMs in improving application efficacies were also demonstrated. In addition, the biological response, from microbial community changes, extracellular polymeric substances changes to biological pathway alteration, may become important in the application of these composites. Furthermore, we also discuss challenges facing the environmental application of GBMs, considering their fate and toxicity in the ecosystem, and offer potential solutions. This research significantly enhances our comprehension of the fundamental principles, underlying mechanisms, and biological pathways for the in-situ utilization of GBMs.

View all citing articles on Scopus

View full text

Bacterial community shift and improved performance induced by in situ preparing dual graphene modified bioelectrode in microbial fuel cell

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

MFC running conditions

General characteristics of the pyrosequencing data

Conclusions

Acknowledgements

Biosens. Bioelectron.

J. Power Sources

Ecol. Eng.

Chemosphere

New. Biotechnol.

Colloids. Surf. B

J. Power Sources

Chemosphere

Int. J. Hydrogen Energy

Renew. Sust. Energy Rev.

Bioresour. Technol.

J. Power Sources

Soil Biol. Biochem.

Trends Microbiol.

Fuel

Int. J. Hydrogen Energy

Bioresour. Technol.

J. Power Sources

Chem. Eng. J.

J. Microbiol. Methods

Soil Biol. Biochem.

Renew. Sust. Energy Rev.

J. Hazard. Mater.

Biosens. Bioelectron.

Appl. Catal. B