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Article

Electrode Microbial Communities Associated with Electron Donor Source Types in a Bioelectrochemical System Treating Azo-Dye Wastewater

by
Zechong Guo
1,2,3,
Lu Zhang
1,
Min-Hua Cui
2,4,* and
Aijie Wang
2,5,*
1
School of Environmental and Chemical Engineering, Jiangsu University of Science and Technology, Zhenjiang 212100, China
2
State Key Laboratory of Urban Water Resource and Environment, Harbin Institute of Technology, Harbin 150090, China
3
Jiangxi Jindalai Environmental Protection Co., Ltd., Nanchang 330100, China
4
School of Environmental and Civil Engineering, Jiangnan University, Wuxi 214122, China
5
Key Laboratory of Environmental Biotechnology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
*
Authors to whom correspondence should be addressed.
Water 2022, 14(9), 1505; https://0-doi-org.brum.beds.ac.uk/10.3390/w14091505
Submission received: 18 March 2022 / Revised: 27 April 2022 / Accepted: 5 May 2022 / Published: 7 May 2022
(This article belongs to the Special Issue The Application of Electrochemical Methods in Water Treatment)
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Abstract

:
Bioelectrochemical systems (BESs) have been acknowledged to be an efficient technology for refractory pollution treatment. An electron donor is as an indispensable element of BES, and domestic wastewater (DW) has been proved as a cost-efficient and accessible alternative option to expensive carbon sources (such as acetate and glucose), yet its effect on microbial community evolution has not been thoroughly revealed. In this study, the electrode microbial communities from BESs treating azo dye wastewater fed by DW (RDW), acetate (RAc), and glucose (RGlu) were systematically revealed based on 16S rRNA Illumina MiSeq sequencing platform. It was found that there were significant differences between three groups in microbial community structures. Desulfovibrio, Acinetobacter, and Klebsiella were identified as the predominant bacterial genera in RDW, RAc, and RGlu, respectively. Methanosaeta, the most enriched methanogen in all reactors, had a relative lower abundance in RDW. Microbial communities in RAc and RGlu were sensitive to electrode polarity while RDW was sensitive to electrode position. Compared with pure substrates, DW increased the diversity of microbial community and, thus, may enhance the stability of electrode biofilm. This study provides an insight into the microbial response mechanism to the electron donors and provides engineering implications for the development of BES.

Graphical Abstract

1. Introduction

Electrochemical technologies are proved as an efficient method for contamination remediation by electrochemical oxidation and electrochemical reduction processes [1,2]. However, the high cost and extreme operating conditions impede wide applications in the practical scene. Considering the cost-efficient and feasibility of large-scale capability, biological treatment is still the most widely used wastewater treatment technology. However, it was difficult to satisfy the stricter discharging standard due to the low efficiency and complicated manipulation, especially in treating refractory industrial wastewaters, such as azo dye wastewater, chemical wastewater, etc. Introducing electrochemical technology into conventional biological facilities seems to be a potential strategy to deal with wastewater issues [3]. The bioelectrochemical system (BES) is a rapidly developing technology that inherits both the advantages of electrochemical and biological processes. The feasibility and superiority of implementing BES to remediate pollution have been verified in covering azo dyes, nitro compounds and metals reduction, and dehalogenation [4]. Among them, azo dye decolorization is one of the most successful applications of BES in industrial wastewater treatments. Due to the presence of external circuit, the electron transfer process was obviously enhanced and resulted in fast decolorization compared to traditional anaerobic process. For now, several pioneer works have confirmed the feasibility of the practical application of BES technology [4]. However, more efforts are required to promote the industrialized application of BES, such as evaluating the performance under practical scenario, exploring the mechanism of microbial functional stabilization, reducing the operational cost of BES technology, etc.
In a BES, electrochemical active microorganisms (EAMs) play an important role by involving extracellular electron transfer. Electrons are produced by anode respiration bacteria oxidizing organic matters and transferred to the cathode to drive reduction actions. These EAMs can serve as a biocatalyst to decrease applied voltage and increase reaction efficiency. Thus, to maintain a stable microbial community structure capable of achieving efficient electron transfer, pollutant degradation is crucial to the successful operation of a BES. In addition to some common physical and chemical influencing factors [5,6,7,8,9,10] in BES, the microbial community structure might also be influenced by some special operation parameters, such as electrode position and polarity [4,11], salinity and COD/N [12], applied voltage [13], organic loading rates, and electron donors. In previous studies, simple and pure carbon sources such as acetate, glucose, and yeast extract are commonly employed to support BES’s operation, but they comprise diseconomy and are impracticable to access in the large-scale application scene. To decrease operating costs, various organic wastes/wastewater were proposed to serve as alternative electron donors to drive bioelectrochemical reactions. Among them, domestic wastewater (DW) has been proved to be a cost-effective yet highly efficient electron donor source in a BES treating azo dye wastewater in our previous study [14]; nevertheless, the characteristics of the microbial community structure of electrode biofilm with DW as a carbon source has not been thoroughly revealed. Therefore, this study systematically analyzed the effects of various electron donors (including acetate, glucose, and DW) on microbial community structure by conducting 16S rRNA Illumina Miseq sequencing and evaluated the feasibility and superiority of DW as electron donor at the level of microbial community evolution.

2. Materials and Methods

2.1. Reactor Configuration and Operation

Three identical cylindrical reactors were manufactured with plexiglass [14]. Each one had a working volume of approximately 1.25 L (ID × L = 8 cm × 25 cm) (see Figure 1). Two pairs of electrodes were installed into the reactor, from the bottom to the top, which was arranged as down-cathode, down-anode, up-cathode, and up-anode with the distance of 2.5 cm between each electrode. Both anodes and cathodes were constructed by granular graphite (diameter from 3 to 6 mm) with 8 cm in diameter and 4 cm in height, producing the total electrode volume of 200 cm3. Before use, granular graphite was washed by soaking in 32% HCl four times to remove foreign materials [15]. The graphite rod (Φ = 4 mm) penetrated the electrode zone and worked as an electron collector. A saturated calomel electrode (SCE, +247 mV vs. standard hydrogen electrode) was used as the reference electrode. During all experiments, a voltage of 0.5 V was supplied between the anode and cathode by a DC power supply. A 10 Ω resistor was connected in series into the electric circuit. The voltages across this resistor were recorded every 10 min by a data acquisition system (Keithley 2700), which were automatically converted to the current according to Ohm law.
All three reactors were startup in batch mode. Effluent collected from a long-term operated single chamber BES was amended with sodium acetate (NaAc, 1000 mg/L) and acid orange 7 (AO7, 200 mg/L) as the inoculum solution. In the first batch operation cycle, 50 mL anaerobic activated sludge (SS of 35.57 mg/L and VSS of mg/L) was also added into the reactors to strengthen the biomass. After that, the inoculum solution was replaced every two days. When a stable current output was observed, the reactors were considered to be successfully started up. Subsequently, the operation of reactors was changed to continuous flow mode. The hydraulic retention times for all reactors were set at 6 h throughout the experiment. Domestic wastewater (DW) collected from a local sewage well was filtered by a 400-mesh sieve to remove particles that might block the interspace of electrodes. The COD of the filtrated DW was detected as 309 ± 18 mg/L in all experiments, total nitrogen of 59.38 ± 1.54 mg/L, ammonium of 49.68 ± 5.29 mg/L, total phosphorus of 13.14 ± 1.43 mg/L, sulfate of 88.90 ± 11.33 mg/L, chloride of 67.41 ± 18.04 mg/L, alkalinity of 217 ± 75 mg-CaCO3/L, and pH of 7.39 ± 0.07. DW was then amended with AO7 (200 mg/L) as the influent of one reactor (RDW). As the controls, the other two reactors were fed with synthetic wastewater with acetate (RAc) and glucose (RGlu) as the electron donor sources, respectively, which contributed the same COD as that in DW. In addition to the electron donor sources, synthetic wastewater comrpised AO7 (200 mg/L) and other minerals, as reported previously [16].

2.2. Chemicals and Analytical Method

The liquid samples were collected every day. AO 7 was used as the model azo dye (purity > 95%, Shanghai Sangon Biotech Co., Ltd., Shanghai, China). Liquid samples taken from reactors were immediately filtered through the 0.45 μm filters (Tianjin Jinteng Experiment Equipment Co., Ltd., Tianjin, China). AO7 concentration was quantified by a UV-Vis spectrophotometer (UV-1800, Shanghai Meipuda instrument Co., Ltd., Shanghai, China) at a wavelength of 484 nm. COD was quantified by the HACH method.

2.3. Biofilm Sampling and High-Throughput 16S rRNA Gene Illumina MiSeq Sequencing

After operating those reactors for more than 200 days, biofilms along with graphite particles were collected from anodes and cathodes, respectively. Graphite particles of each electrode were sampled from at least 6 positions in different heights and combined for DNA extraction.
Amplicon libraries were constructed by Illumina Miseq PE 250 using universal primers 515F (5′-GTGCCAGCMGCCGCGGTAA-3′) and 806R (5′-GGACTACHVGGGTWTCTAAT-3′). Both forward and reverse primers were added with barcodes. PCR amplification, products purification and quantification, and sequencing were carried out by using the Illumina MiSeq platform in The Beijing Genomics Institute (BGI).

3. Results and Discussion

3.1. Performance of BESs Served with Different Electron Donor Source

The BESs fed with domestic wastewater (RDW), glucose (RGlu), and acetate (RAc) presented similar and commendable decolorization efficiency (>98%) with azo dye AO 7 loading rates increased from 200 to 800 g/(m3·d). The COD consumptions among the three reactors were significantly different despite influent COD concentrations being controlled at a parallel level. The highest COD removal efficiency of RAc was 39.89 ± 1.95% followed by RGlu of 34.01 ± 2.20%, and lowest COD removal efficiency was recorded in RDW (19.56 ± 3.21%). Given the different yet similar electrons from COD oxidation used for azo dye decolorization, RDW showed the highest electrons utilization efficiency. In RGlu and RAc, more electrons were lost in the unwanted parallel routes, such as biomass production and methanogenesis. By decreasing electron donor concentrations from 300 to 80 mg-COD/L, the decolorization efficiencies of RGlu and RAc obviously deteriorated to 85.85 ± 2.33% and 72.41 ± 1.37%, respectively, which was still kept at 94.91 ± 1.55% in RDW. The preferable performance of RDW under lower electron donation conditions emphasized that DW could serve as a cost-efficient electron donor source to drive BES for implementing the decolorization of azo dye [14].

3.2. Overall Microbial Community Structures

Illumina sequencing platform was employed to analyze microbial communities from 12 electrode biofilms of three reactors, the nomenclature and alpha diversity were shown in Table 1. Approximate 30,000 high-quality sequences were obtained from each sample (Figure 2). Significantly more operational taxonomic units (OTUs) were observed in samples fed with DW, followed by glucose and acetate, respectively. It indicated that microbial diversity highly depended on the complexity of the electron donor source. The estimated species richness abundance-based coverage estimator (ACE) and Chao1 were also consistent with this trend, which was significantly higher in RDW samples than that in RAc and RGlu (p < 0.05). It implied that more species were found in RDW. Shannon index was employed to evaluate the evenness of the samples and reflected that the microbial communities from RDW showed better evenness. It was also confirmed by the lowest Simpson index obtained in RDW samples.
Principal component analysis (PCA) demonstrated that samples from the same reactor clustered together and presented high similarity of the microbial communities (Figure 3). It is reasonable considering the process of varied electron donor source utilization. Acetate is the simplest one and can be directly utilized as an electron donor. Glucose would be fermented into volatile fatty acids and then be utilized by microbes. DW metabolic processes involve hydrolysis, acidogenesis, acetogenesis, and methanogenesis, which are operated by diverse consortia.
Hierarchical cluster analysis was used to identify the differences of 12 microbial communities, as shown in Figure 4. Overall, microbial communities from RAc and RGlu were relatively similar and separated from the RDW group, suggesting clear distinctions of community structure between the complex feeding reactor and simple one. This was consistent with PCA results. In RAc and RGlu, the microbial communities from the same polarity of electrode biofilm clustered together even though they were located in a different position. It indicated that the electrode polarity was the major influence factor on the microbial community structures from electrode biofilms in RAc and RGlu. It was different in RDW where position rather than polarity seems to be the dominant influence factor on the microbial communities. It can be deduced that the electron donor source was a dominant factor that influenced the microbial community structure of electrode biofilms. Simple carbon source (NaAc and glucose) was more likely to be utilized by electricigens, which led to a decrease in diversity and an increase in similarity of biofilm microbial community structure. While serving a complex carbon source (DW), electron production requires a long and complicated metabolic pathway constructed by a more diversified microbial community structure.

3.3. Microbial Community Structures at Phylum, Class, and Family Levels

Microbial community structures from 12 samples were compared at phylum, class, and family levels (Figure 5). As it can be seen, the carbon source significantly altered the microbial community structure. A total of 11 phyla with relative abundance >1% were identified as shown in Figure 5A. Bacteroidetes, Firmicutes, and Proteobacteria were the dominant member. Bacteroidetes was the most enriched phylum in RDW with an average abundance of 31.92 ± 3.31%, which was followed by 7.15 ± 1.99% and 11.52 ± 3.22% in RAc and RGlu, respectively. Bacteroidetes were widely reported in BESs [17]. Firmicutes were enriched in RGlu with a relative abundance of 32.65 ± 7.18%. Firmicutes were frequently identified from BES that fed glucose as a carbon source [18,19]. Proteobacteria were the absolute dominant phylum in RAc (47.22 ± 18.13%), which were 29.69 ± 11.45% and 29.67 ± 17.59% in RDW and RGlu, respectively. In addition, Synergistota was the other relative enriched phylum with the abundances of 3.96 ± 0.98, 2.64 ± 2.84, and 1.31 ± 1.12% in RDW, RAc, and RGlu, respectively. It is worth noting that Synergistota seems to be enriched in the anode biofilm. Especially in RAc and RGlu that feed with a simple carbon source, the relative abundance of Synergistota in the anode biofilm was one order of magnitude higher than the corresponding cathode. It seems to imply that the phylum of Synergistetes was relevant to the anodic respiration and extracellular electron transfer; however, there was no solid evidence to confirm this, and a deep investigation is required for illumination. A total of 18 classes were identified from 12 biofilm samples (relative abundance >1%, as shown in Figure 5B). Δ-proteobacteria with the relative abundance of 23.23 ± 11.12% was the dominant member and followed by γ-proteobacteria (5.48 ± 1.06%) in biofilms from RDW, and γ-proteobacteria was the dominant class in RAc (33.46 ± 12.95%). While Bacilli, γ- and δ-proteobacteria were found to be the dominant member in biofilms in RGlu with a relative abundance of 22.40 ± 9.67%, 18.23 ± 13.33%, and 9.89 ± 2.93%, respectively.

3.4. Potential Function of Dominant Genera

An in-depth characterization of microbial community was performed at a genus level. Thirty-one genera with relative abundance >1% in the twelve microbial communities are shown in Table 2. Geobacter, a typical exoelectrogen, was found to be the dominant member in all anodic biofilms with the relative abundance in a range of 6.75% and 14.15%, which was higher than their corresponding cathodic biofilms. Geobacter sulfurreducens was the first reported strain in which microbial electricity production occurred solely by cells attached to an electrode [20]. In addition, the azo dye reduction capability of Geobacter has also been discovered [21].
In the RDW group, Desulfovibrio was enriched (13.96, 11.99, 6.30, and 8.31%) compared to RAc and RGlu. Desulfovibrio has been proved as a functional genus for extracellular electron transfer (EET) and azo dye reduction [22,23]. It was interesting that the Desulfovibrio relative abundance of the microbial community was more sensitive to the electrode position rather than polarity, which was selectively enriched in the biofilms collected from down position electrodes. It is reasonable considering that this genus can grow with a broad range and as complex organic matters with electron donors [24], and it is adaptable to the complex composition of DW.
Acinetobacter is non-fermentive and capable of growth in mineral media with acetate as the sole carbon source [25]. It seems to be the reason that Acinetobacter was the dominant member in all samples from the RAc group. Acinetobacter was selectively enriched in anodic biofilm with relative abundances of 32.89 and 38.51%, which decreased to 18.76 and 18.26% in cathodic ones. It strongly implied that Acinetobacter was involved in electrode respiration; however, we failed to find out an explicit report to confirm the direct link between Acinetobacter and EET. Acinetobacter presented function in azo dye decolorization [26]. Pseudomonas, a reported exoelectrogen as well as an azo dye decolorizing genus, was selected enriched in anodic biofilms (7.80% and 8.35%) versus cathodes (2.05% and 5.21%), which can produce phenazine-based metabolites to stimulate EET [27,28]. In addition, Arcobacter was another exoelectrogen that had high relative abundances in RAc electrodes (1.09%, 5.14%, 1.23%, and 8.76%). It has been verified that they were neither fermented nor oxidized carbohydrates, yet organic and amino acids could be utilized as carbon sources [29,30].
In the RGlu group, Klebsiella was the dominant member with relative abundances of 17.43% and 15.33% in anodes and one order of magnitude lower (3.24% and 2.44%) in cathodes. It is a functional genus of EET and azo dye reduction [31,32]. Acetobacterium was an enriched genus in RGlu group, with relative abundances of 4.87%, 7.27%, 3.28%, and 1.22%. Acetobacterium was not proved for its function in EET or azo dye reduction; however, it was an acetogenic microbe and can produce acetate by oxidizing glucose [33].
In terms of archaea, Methanosaeta was the predominant methane producer that specializes in only using acetate for methane production. No growth on or methane production from H2/CO2, formate, methanol, ethanol, trimethylamine, isobutanol, or isopropanol [34] was observed. This explains the enrichment of Methanosaeta on the RAc biofilms (37.25%, 26.26%, 35.83%, and 15.43%). The relative abundances of Methanosaeta were lower in the RDW and RGlu groups and relatively enriched in the down electrode biofilms. Both DW and glucose should be fermented in acetate to create a favorable condition for Methanosaeta metabolism so that they are relatively enriched on the up electrodes. The recent literature indicated Methanosaeta is able to acquire electrons from exoelectrogen (e.g., Geobacter) by direct interspecies electron transfer process [35,36]. In addition, Methanosaeta was found to be a dominant member in a microbial community from an anaerobic baffled reactor treating dyes wastewater, which implied it could tolerate the toxicity of the dyes and possibly be involved in dye removal. Other methane producers, Methanobacterium, Methanocorpusculum, Methanosarcina, and Methanospirillum, were found but with quite lower relative abundances in 12 biofilms.
Canonical correspondence analysis (CCA) was employed to evaluate the effect of electron donor source types on the microbial community structures, as shown in Figure 6. The arrow direction of acetate was positively correlated with the horizontal canonical axis, and DW and glucose were located in the middle of the second and third quadrant of the cartesian coordinate. The separation of three electron donor sources indicated the relatively independent selective pressure. Mangroviflexus stood in the DW direction and far away from the origin, and its enrichment was highly sensitive to DW. It was a dominant genus in the rural household biogas digesters and played a crucial role in reducing and oxidizing reactions to bio-degrade organic matters [37]. Parabacteroides was an obligately anaerobic species from wastewater of a paper mill [38]. Desulfuromonas was able to oxidize complex organics such as long-chain fatty acids and use tetrachloroethylene, trichloroethylene, and Fe(III) as electron acceptors [39,40]. Klebsiella had a function of EET from glucose oxidation [41]; thus, it was enriched on the anodes from RGlu. Acinetobacter, Arcobacter, and Flavobacterium were highly sensitive to the acetate.
The comparisons of the dominant genera that were identified from BESs fed with various electron donor sources are summarized in Table S1 [42,43,44,45]. It is quite clear that the genera with a function of extracellular electron transfer, such as Geobacter, Pseudomonas, Desulfovibrio, and Klebsiella, were enriched in the electrode microbial community. Those genera seemed to endow an electrochemical activity of the electrode biofilms. Specific genus was enriched based on the characteristics of the substrate. Comamonadaceae was enriched in a BES with phenol as the substrate [45], and Klebsiella was enriched in this work with domestic wastewater as the electron donor.

4. Conclusions

Employing domestic wastewater as electron donor source to drive bioelectrochemical reaction was feasible and cost-efficient. In this study, the electrode microbial communities from bioelectrochemical systems fed with domestic wastewater (RDW), acetate (RAc), and glucose (RGlu) were systematically revealed. Similar decolorization performances were observed among three BESs, while the microbial community structures were quite different. Microbial diversity highly depended on the complexity of the electron donor source, and significantly more OTUs were observed in RDW compared to RGlu and RAc. Bacteroidetes, Firmicutes, and Proteobacteria were identified as the dominated phyla in RDW, RGlu, and RAc, respectively. Desulfovibrio, Acinetobacter, and Klebsiella were identified as the predominant bacterial genera in RDW, RAc, and RGlu, respectively. Typical exoelectrogen Geobacter was found to be enriched in the anodes’ biofilms among three BES reactors. Methanosaeta was the most enriched methanogen in all reactors. This study provides an insight in the microbial response mechanism to the electron donor sources and provides great inspiration to bring bioelectrochemical technology closer to applications.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/w14091505/s1, Table S1: Comparison of dominant genera fed with various electron donor sources.

Author Contributions

Z.G.: Investigation, funding acquisition, and writing—review and editing. L.Z.: Investigation and writing—original draft. M.-H.C.: Conceptualization, funding acquisition, and writing—review and editing. A.W.: Project administration and supervision. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Natural Science Foundation of Jiangsu Province, No. BK20190980; the National Natural Science Foundation of China, No. 52000090 and 52000088; the China Postdoctoral Science Foundation, No. 2021M701511; the Open Project of Key Laboratory of Environmental Biotechnology, CAS, Grant No. kf2020010.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Water 14 01505 g001 550
Figure 1. Schematic representation of the reactor [14].
Figure 1. Schematic representation of the reactor [14].
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Figure 2. Rarefaction curves of the microbial communities.
Figure 2. Rarefaction curves of the microbial communities.
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Figure 3. Principal component analysis (PCA) of microbial communities from different electron donor sources feeding BESs.
Figure 3. Principal component analysis (PCA) of microbial communities from different electron donor sources feeding BESs.
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Figure 4. Hierarchical cluster analysis of microbial communities 12 biofilm samples.
Figure 4. Hierarchical cluster analysis of microbial communities 12 biofilm samples.
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Figure 5. Microbial community comparison at phylum (A) and class (B) level.
Figure 5. Microbial community comparison at phylum (A) and class (B) level.
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Figure 6. Canonical correspondence analysis for electron donor sources and functional genera from electrode microbial communities.
Figure 6. Canonical correspondence analysis for electron donor sources and functional genera from electrode microbial communities.
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Table
Table 1. Nomenclature and alpha diversity of 12 microbial communities.
Table 1. Nomenclature and alpha diversity of 12 microbial communities.
MarkSample NameNumber of SequencesOTUChao 1ACEShannonSimpson
C1RDW down-cathode29,5146496997154.290.04
C2RDW down-anode28,7866256626824.230.04
C3RDW up-cathode31,2815395926093.670.07
C4RDW up-anode30,2245776296443.790.06
C5RAc down-cathode33,0333353563732.800.17
C6RAc down-anode34,7603464004083.100.11
C7RAc up-cathode35,1823984684553.120.15
C8RAc up-anode33,8103513884153.300.08
C9RGlu down-cathode32,1823764214383.230.13
C10RGlu down-anode30,7763874644693.630.06
C11RGlu up-cathode31,6873543833933.300.12
C12RGlu up-anode31,2574024634833.290.10
Table
Table 2. Microbial community comparison at genus level.
Table 2. Microbial community comparison at genus level.
GenusC1C2C3C4C5C6C7C8C9C10C11C12
Methanosaeta0.70 0.27 19.0016.4637.2526.2635.8315.4317.294.84 18.9418.51
Acinetobacter1.53 1.67 1.68 2.03 18.7632.8918.2638.510.74 2.57 1.38 2.50
Pseudomonas0.55 0.48 0.51 0.86 2.05 7.805.218.350.59 4.99 1.46 3.54
Geobacter1.65 14.150.46 11.841.71 8.350.35 6.750.26 8.020.12 7.68
Arcobacter0.04 0.08 0.04 0.08 1.09 5.141.23 8.760.07 0.75 0.11 0.32
Thermovirga0.16 0.03 2.16 1.86 6.340.16 1.98 0.29 0.47 0.09 0.52 0.07
Desulforhabdus0.19 0.32 1.49 1.73 4.90 0.76 2.70 0.28 0.31 0.01 0.39 0.14
Desulfovibrio13.9611.996.308.311.88 0.16 2.00 0.26 4.71 4.84 6.502.23
Desulfobulbus4.34 3.82 0.15 2.16 0.29 0.07 0.18 0.07 1.00 0.55 0.51 0.36
Methanobacterium0.26 0.04 8.070.03 0.05 0.02 1.04 0.04 0.43 0.07 1.81 0.45
Parabacteroides2.19 3.51 0.88 1.32 -0.02 0.01 0.01 0.15 0.36 0.10 0.13
Desulfuromonas0.12 3.93 0.36 2.90 0.02 0.00 0.01 0.04 0.48 0.05 0.24 0.01
Klebsiella1.24 0.82 1.07 0.78 0.02 0.04 0.04 0.01 3.24 17.432.44 15.33
Acetobacterium1.30 1.65 0.17 0.51 --0.00 -4.87 7.273.28 1.22
Aeromonas2.52 1.04 0.82 0.69 0.02 0.21 0.05 0.13 0.89 4.03 0.62 3.16
Denitrovibrio-0.02 -0.02 0.01 0.03 0.01 0.02 0.04 5.94 0.01 1.01
Fusibacter0.31 0.54 0.29 0.20 0.04 0.70 0.17 0.21 0.08 3.41 0.12 2.94
Proteiniphilum1.00 0.52 2.35 1.86 0.30 0.43 0.48 0.13 1.01 0.18 2.22 0.17
Cloacibacillus1.40 1.18 1.04 0.57 0.19 0.32 0.71 0.20 1.17 0.16 1.91 0.23
Mangroviflexus2.58 0.39 0.10 0.06 -----0.01 --
Anaerovorax1.22 0.56 0.73 0.51 0.52 0.38 0.60 0.48 0.23 0.19 0.14 0.12
Methanocorpusculum2.02 0.29 -0.01 0.01 0.00 0.04 0.00 1.12 0.10 0.18 0.09
Methanosarcina1.05 0.20 0.17 0.63 2.76 0.49 0.29 0.56 0.06 0.01 0.10 0.02
Shewanella0.53 0.50 0.32 0.22 0.03 0.14 0.09 0.13 0.80 2.38 0.62 1.50
Comamonas0.31 0.43 0.13 0.31 0.32 0.56 0.26 2.08 0.08 0.49 0.11 0.65
Methanospirillum0.24 0.01 0.89 0.00 0.04 0.01 0.25 0.00 1.82 0.19 0.97 0.06
Lactococcus0.09 0.07 0.10 0.15 0.47 1.44 2.11 1.62 0.14 0.41 0.60 0.93
Bacteroides0.10 0.15 0.03 0.03 -0.00 0.02 0.01 0.29 1.16 0.21 0.65
Bacillus0.04 0.05 0.04 0.13 0.42 1.31 2.00 1.44 0.06 0.34 0.79 1.03
Sulfurospirillum0.07 0.02 0.02 0.01 0.00 0.00 --0.03 1.59 0.01 0.09
Flavobacterium0.04 0.03 0.01 0.03 0.12 0.69 0.33 2.89 0.02 0.08 0.03 0.06
Unclassified49.70 44.25 43.67 36.64 15.93 8.01 18.17 7.63 49.76 21.83 47.64 28.93
Others # (<1%)8.53 6.99 6.95 7.09 4.48 3.59 5.58 3.66 7.80 5.69 5.89 5.85
Dominant genera (>5%) in electrode biofilms were bolded; #: genus relative abundance less than 1% were classified as “Others”; “0.00”: genus that identified yet low relative abundance; “-”: genus that were undetected in electrode biofilms.
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Guo, Z.; Zhang, L.; Cui, M.-H.; Wang, A. Electrode Microbial Communities Associated with Electron Donor Source Types in a Bioelectrochemical System Treating Azo-Dye Wastewater. Water 2022, 14, 1505. https://0-doi-org.brum.beds.ac.uk/10.3390/w14091505

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Guo Z, Zhang L, Cui M-H, Wang A. Electrode Microbial Communities Associated with Electron Donor Source Types in a Bioelectrochemical System Treating Azo-Dye Wastewater. Water. 2022; 14(9):1505. https://0-doi-org.brum.beds.ac.uk/10.3390/w14091505

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Guo, Zechong, Lu Zhang, Min-Hua Cui, and Aijie Wang. 2022. "Electrode Microbial Communities Associated with Electron Donor Source Types in a Bioelectrochemical System Treating Azo-Dye Wastewater" Water 14, no. 9: 1505. https://0-doi-org.brum.beds.ac.uk/10.3390/w14091505

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