Carbon cloth enhances treatment of high-strength brewery wastewater in anaerobic dynamic membrane bioreactors

Journal Pre-proofs Carbon cloth enhances treatment of high-strength brewery wastewater in anaerobic dynamic membrane bioreactors Ruixue Jia, Dezhi Sun, Yan Dang, David Meier, Dawn E. Holmes, Jessica A. Smith PII: DOI: Reference:

S0960-8524(19)31777-8 https://doi.org/10.1016/j.biortech.2019.122547 BITE 122547

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Bioresource Technology

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29 September 2019 29 November 2019 30 November 2019

Please cite this article as: Jia, R., Sun, D., Dang, Y., Meier, D., Holmes, D.E., Smith, J.A., Carbon cloth enhances treatment of high-strength brewery wastewater in anaerobic dynamic membrane bioreactors, Bioresource Technology (2019), doi: https://doi.org/10.1016/j.biortech.2019.122547

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Carbon cloth enhances treatment of high-strength brewery wastewater in anaerobic dynamic membrane bioreactors Ruixue Jiaa, Dezhi Suna, Yan Danga*, David Meierd, Dawn E. Holmesc, Jessica A. Smithb

a Beijing

Key Laboratory for Source Control Technology of Water Pollution,

Engineering Research Center for Water Pollution Source Control and Ecoremediation, College of Environmental Science and Engineering, Beijing Forestry University, Beijing, 100083, China b

Department of Biomolecular Sciences, Central Connecticut State University, 1615

Stanley Street, New Britain, CT 06050, USA c Department

of Physical and Biological Sciences, Western New England

University, 1215 Wilbraham Rd, Springfield, MA 01119, USA d

School of Natural Science, Hampshire College, 893 West St, Amherst, MA 01002,

USA

*Corresponding authors Yan Dang, College of Environmental Science & Engineering, Beijing Forestry University, 35 Tsinghua East Road, Beijing 100083, China. (E-mail: [email protected])

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ABSTRACT: Anaerobic dynamic membrane bioreactors (AnDMBR) can improve the efficiency of organic matter removal during wastewater treatment at a low cost. However, application of AnDMBRs for treatment of high-strength wastewater is usually unsuccessful. This study investigated whether use of conductive carbon cloth as the supporting material in an AnDMBR permits higher organic loading rates for treatment of brewery wastewater than non-conductive polyester cloth. The AnDMBR with carbon cloth operated stably with a COD removal efficiency of 98% even when high concentrations of influent COD (10,000 mg/L) were provided, while the polyester cloth reactor deteriorated when reactors were fed only 5000 mg/L influent COD. Microorganisms capable of direct interspecies electron transfer (DIET), including Geobacter and Methanothrix species, dominated the surface of the carbon cloth. These results demonstrate that carbon cloth provides an excellent supporting material for AnDMBR by stimulating growth of microorganisms that can directly transport electrons to and from conductive materials.

Key words: Anaerobic dynamic membrane bioreactors; Carbon cloth; Direct interspecies electron transfer; Supporting material; High-strength brewery wastewater

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1. Introduction Globally, the brewing industry is responsible for production of a significant amount of high pollution wastewater. In fact, it has been estimated that for every liter of beer, 3–10 L of waste effluent is generated (Simate et al., 2011). Brewery wastewater contains large quantities of organic matter (sugar, soluble starch, ethanol, volatile fatty acids, etc.) (Wang et al., 2008), and suspended solids (SS) (i.e. spent maize, malt, and yeast) (Parawira et al., 2005), which results in chemical oxygen demands (COD) of 20,000-60,000 mg/L, SS levels of ~3000 mg/L, and biochemical oxygen demand (BOD)/COD ratios of 0.5-0.7 (Morita et al., 2011; Rao et al., 2007). If discharged directly, this wastewater can cause considerable environmental damage particularly through eutrophication of water bodies (Qin, 2018). Therefore, development of suitable treatment methods is an important area of research. Anaerobic digestion, a process that converts the chemical energy stored in organic compounds into biogas, is one of the primary methods used to treat brewery wastewater (Holmes & Smith, 2016; Parawira et al., 2005; Rao et al., 2007). The natural properties of brewery wastewater can provide ideal conditions for anaerobic digestion (Parawira et al., 2005). However, promoting the growth of anaerobic microorganisms and retaining biomass remain significant challenges. Anaerobic membrane bioreactors (AnMBR) can be used to retain biomass and promote energy production during anaerobic treatment by adding membrane filters that separate solids and liquids. A more advanced technology derived from AnMBR, known as anaerobic dynamic membrane bioreactor (AnDMBR), utilizes supporting materials

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such as mesh or filter cloth in place of standard membrane filters. Unlike more traditional filters, mesh and filter cloth promote the formation of cake layers, which are primarily composed of microbial products and extracellular polymeric substances (EPS). Cake layers enhance solid-liquid separation in the bioreactor because they can be easily removed from the supporting material (Ersahin et al., 2014; Xie et al., 2014). This low-cost method has been shown to efficiently remove several pollutants, including COD and SS, from wastewater without aeration (Alibardi et al., 2016; Ersahin et al., 2014; Xie et al., 2014). Most of the currently published AnDMBR studies used simple feeding wastewater such as low-concentration urban sewage (An et al., 2009; Liu et al., 2016; Ma et al., 2013a; Ma et al., 2013b; Quek et al., 2017; Zhang et al., 2010; Zhang et al., 2011) or simulated wastewater containing highly degradable organics like acetate (Ersahin et al., 2014; Ersahin et al., 2017) or sucrose (Alibardi et al., 2016). There have been few investigations into the use of high-strength wastewater treatment by AnDMBR. In addition, these previous studies used porous supporting materials such as polyester, dacron, polypropylene, and nylon which can be unstable and tend to have short lifespans (Cayetano et al., 2019; Ersahin et al., 2017; Hu et al., 2018; Saleem et al., 2018). Conductive carbon cloth is a promising alternative to these materials as it is costeffective, light-weight, high-strength, corrosion resistant, age-resistant, durable, and physically stable (Dang et al., 2017; Sasaki et al., 2007; Zhao et al., 2015). Addition of carbon cloth to bioreactors has also been shown to support biofilm growth and enhance anaerobic digestion of organic wastes to methane (Sasaki et al., 2007).

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One of the primary ways carbon cloth enhances anaerobic digestion is by promoting direct interspecies electron transfer (DIET) between bacteria and methanogens (Chen et al., 2014). DIET occurs when electrons are transferred by direct connections between two microorganisms via protein appendages such as electrically conductive pili (e-pili) and outer cell surface c-type cytochromes, without the involvement of soluble electron carriers (Rotaru et al., 2014b). DIET is accelerated when electrons are directly transferred to and from non-biological conductive materials such as carbon cloth (Zhao et al., 2015), which enhances methane production, reduces reaction time, and improves COD removal efficiencies in anaerobic digesters, particularly at high organic loading rates (Dang et al., 2016b; Lei et al., 2016; Zhao et al., 2015). Based on these prior studies, it is proposed that the use of conductive carbon cloth as the supporting material for AnDMBR should enhance wastewater treatment efficiencies. In this study, AnDMBRs were used to treat high-concentration refractory brewery wastewater with either conductive carbon cloth or polyester cloth added as the supporting material. COD removal, ethanol concentrations, and methane production rates were compared for the two reaction systems in order to assess treatment efficiencies. In addition, bacterial and archaeal communities associated with the carbon or polyester cloth surfaces and reactor sludge were compared.

2. Material and methods 2.1 Reactor design

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Two laboratory-scale continuous-flow AnDMBRs were operated in parallel for this study. Fig. 1 displays a schematic diagram of the AnDMBR systems, which consisted of plexiglass reactors with a working volume of 6.8 L and a submerged flat sheet membrane module (Ersahin et al., 2014). Either conductive carbon cloth or nonconductive polyester cloth was provided as supporting material in the membrane module. The total area on both sides of the supporting membrane materials was 0.018 m2, with a mesh pore size of 200 µm. An effluent port and a gas outlet port were constructed on top of the reactor, and an inlet port and two gas circulation ports were constructed at the bottom of the reactor. Biogas aeration pipes were installed at both the bottom of the reactor interior and in the membrane module (Fig. 1). A temperature control device was placed in the middle of the reactor, and all experiments were conducted at 35˚C. Wastewater influent entered from the bottom of the reactor and effluent exited from the top. A portion of gas was collected at the top of the reactor in a gas-sampling bag, while a diaphragm vacuum pump (JINTENG GM-0.20) operating at 400 mL/min allowed re-circulation of the remaining gas within the reactor. Part of the circulating gas was used to evenly mix liquid in the reactor, while the other portion was used at the lower aeration pipe of the membrane module to control dynamic film thickness. 2.2 AnDMBR experimental operation The AnDMBRs were inoculated with anaerobic sludge obtained from an anaerobic digester operating at a municipal wastewater treatment plant. Total suspended solid (TSS) content in the seed sludge was about 26,000 mg/L and the ratio of volatile

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suspended sludge (VSS) to TSS was 0.81. All reactors were fed artificial wastewater prepared as previously described (Morita et al., 2011). Each liter of wastewater contained: 0.6 ml-6.1 ml ethanol, 0.23g urea, 0.11g KH2PO4, 0.17g K2HPO4, 0.05g Na2SO4, 0.1g MgCl2·6H2O, 0.05g CaCl2·2H2O, 10 ml trace element solution, and 10 ml vitamin solution. Trace element and vitamin solutions were prepared as previously reported (Morita et al., 2011; Zhao et al., 2015). Ethanol was the main carbon source in this artificial wastewater, and each ml of ethanol provided a COD of ~1644 mg/L. At the start of the experiment, the inlet water COD was 1000 mg/L, and inflow organic load was gradually increased as the operation stabilized. Maximum load and treatment effects were determined for the reactors. The hydraulic retention time (HRT) of both reactors was 5 days and the sludge retention time (SRT) was 30 days. The entire experimental process included filtration and backwashing, which were carried out by changing the inlet and outlet water direction. AnDMBR operation was conducted at a flux rate of ~4.125 L/(m2h), a backwash step of ~30 min/d, and a biogas sparging rate set at 31.35 m/h. Membrane clogging was monitored with a pressure gauge at the outlet. The membrane was replaced when the pressure difference of the trans membrane was higher than 0.4 bar, the penetration rate was lower than 15L/(m2h), and treatment was insufficient (COD removal efficiency was lower than 40%). 2.3 Analytical methods COD removal efficiencies, methane production rates, pH, effluent ethanol, TSS, VSS, and volatile fatty acids (VFAS) were monitored throughout the study. Soluble chemical oxygen demand (SCOD), total chemical oxygen demand (TCOD) and solids

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(TSS and VSS) were measured according to standard methods (APHA, 2005). The pH was measured using a pH analyzer (UB-10; Denver Instrument; Denver). Transmembrane pressure (TMP) was measured with a pressure sensor located on the dynamic membrane outlet. Biogas volume was recorded with a plastic 100 mL syringe every 24 h and methane content in the biogas was analyzed by a gas chromatograph with a flame ionization detector (Techcomp GC7900). Ethanol concentrations were measured with a gas chromatograph equipped with a headspace sampler and a flame ionization detector (Agilent Technologies 7890A GC System). VFA concentrations were determined by high-performance liquid chromatography (HPLC) (HITACHI Primaide organizer) based on previous methods (Nevin et al., 2010). 2.4 Microbial community analysis and screening for extracellular electron transfer Sludge samples (1.0 g) and biomass collected from carbon cloth and polyester cloth surfaces were collected at the end of digestion while reactors were still in stable condition (carbon cloth reactor on day 45 and control reactor on day 20). All samples were washed with 2.0 ml of phosphate-buffered saline (PBS; 0.13 M NaCl and 10 mM Na2HPO4 at pH 7.2) and then centrifuged at 4000 rpm for 2 min to remove any residual suspended sludge. The pellets were stored at -20˚C. Genomic DNA was extracted with the BIO101 Fast DNA soil kit (MP Biomedicals, Ohio) according to the manufacturer’s instructions. DNA concentration and purity of each sample was then determined with a Nanodrop UV spectrophotometer (Thermo Fisher Scientific, Wilmington, DE, USA). Bacterial and archaeal 16S rRNA gene fragments were amplified via the

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polymerase chain reaction (PCR) with the primer set 338F/524R (Wu et al., 2015). Amplicons were sequenced on an Illumina Hiseq 2000 platform (Illumina, San Diego, CA, USA) by Allwegene Co., Ltd. (Beijing, China). Sequences were placed into various operational taxonomic units with Pyrosequencing Pipeline software (https://pyro.cme.msu.edu). 3. Results and discussion 3.1 Performance of AnDMBRs Two AnDMBRs were operated, one with carbon cloth (CC) and one with polyester cloth (PC), in order to compare the impact that each supporting material might have on brewery wastewater treatment. To assess reactor performance, COD (Fig. 2A) and methane production (Fig. 2B) were monitored throughout the course of operation. During the initial 20 days of the experiment, influent COD was incrementally increased from 1000 to 3000 mg/L, and both reactors operated efficiently with similar methane production rates (Fig. 2, p > 0.05). However, once inlet COD concentrations increased to > 5000 mg/L (organic loading rate (OLR) 1.115 kg COD/m3/d), the COD removal rate of PC dropped significantly and methane production rates were less than 30 mL (STP)/h. Conversely, CC continued to operate well, and methane production rates spiked to over 80 mL (STP)/h. In fact, methane production rates continued to increase in CC until influent COD concentrations reached 10,000 mg/L. At this point, methane conversion dropped to 20 mL (STP)/h and COD removal rates dropped to 75% (p < 0.01). Effluent ethanol concentrations (Fig. 3A), the concentration of VFAs (acetate,

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propionate, and butyrate) (Fig. 3B), and pH (see Supplementary Material) were also monitored in CC and PC AnDMBRs. For the first 20 days, effluent pH remained stable at 7.8, ethanol content stayed low, and VFAs were not detected in either reactor (Fig. 3, p > 0.05). Once COD removal rates in PC dropped below 75% (Fig. 2A), the effluent pH dropped to 5.8 (see Supplementary Material), and acetate and propionate accumulated (Fig. 3B). CC remained stable until COD concentrations reached 10,000 mg/L around day 40, at which point the pH dropped below 6 (see Supplementary Material), and acetate and butyrate accumulated (Fig. 3B, p < 0.01). Although propionate accumulated significantly in PC, little was detected in CC, and other VFAs were not detected in CC until COD levels reached 10,000 mg/L. These results were similar to a study that showed addition of conductive biochar to bioreactors enhanced propionate degradation (Zhao et al., 2016a). Overall, the CC reactor operated better than the PC reactor, and tolerated substantially higher OLRs (10,000 vs 5000 mg/L COD) (Fig. 2A). CC OLR (2.23 kg COD/m3d) was also greater than many of the previously reported maximum rates tolerated by AnDMBRs treating diverse types of wastewater with other varieties of supporting materials (see Supplementary Material). For example, when polypropylene was used as an AnDMBR supporting material for treatment of high-strength wastewater, the maximum OLR was 2.01 kg COD/m3d (Ersahin et al., 2014). Support materials with large pore sizes such as nylon mesh (Yu et al., 2019) or polyamide/nylon (Alibardi et al., 2016) have often resulted in lower AnDMBR performance. A recent study investigating AnDMBR treating high strength wastewater found

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that use of mesh with the smallest pore size of 10 µm allowed significantly higher COD removal efficiencies than mesh with a 70 µm pore size (Paçal et al., 2019). Both the carbon and polyester cloths used in this study contained a pore size of 200 µm, indicating that other differences in the material (i.e. conductivity) and not pore size contributed to the superior performance of the CC reactor. 3.2 Filtration performance of AnDMBRs During the AnDMBR process, a biological cake layer formed on the carbon and polyester cloth. TMP (Fig. 4A) and solids content (Fig. 4B) measurements were used to assess filtration performance in CC and PC. TMP followed a stable trend that fluctuated between 0 and -0.2 bar, and it only took about 5 days to form reliable dynamic membranes (Fig. 4A). Stable TMPs in this range are correlated with good permeate quality (Guan et al., 2018). During the first 5 days of operation, effluent SS for CC decreased from 55 mg/L to 10 mg/L and PC decreased to 20 mg/L (Fig. 4B). SS for both reactors eventually decreased to nearly 0 mg/L (p > 0.05). VSS/TSS ratios were over 0.70 in both AnDMBR reactors (Fig. 4B). These results correspond with previous studies that have demonstrated that high SS removal efficiencies (up to 99% COD) can be achieved with AnDMBRs (Ersahin et al., 2014; Ersahin et al., 2017). Studies have shown that a high food/microorganism (F/M) ratio, which represents the ratio between COD loaded in the bioreactor and the TSS concentration, can increase the rate of membrane fouling (Trussell et al., 2006). However, F/M ratios did not appear to significantly impact permeate quality in either the CC or PC reactor (Fig. 4B). These

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results further confirm that AnDMBRs can discharge higher-quality effluent compared to other anaerobic treatment processes, including conventional anaerobic digestion (Ersahin et al., 2014; Ersahin et al., 2017; Xie et al., 2014). The fact that there was no significant difference in TMP or effluent SS between the two reactors (Fig. 4, p > 0.05) indicates that both supporting materials promoted similar microbial biomass formation. This suggests that enhanced COD removal and methane production by CC (Fig. 2) was not due to better microbial surface attachment, rather it was the conductive nature of the carbon cloth that led to improved reactor performance (Zhao et al., 2015). 3.3 Microbial community analysis After 55 days of operation, samples were collected from the CC and PC AnDMBRs for bacterial (Fig. 5) and archaeal (Fig. 6) high-throughput 16S rRNA sequence analyses. Samples were collected from biofilms on the carbon cloth (CC-S) or polyester cloth (PC-S), as well as suspended reactor sludge from both AnDMBRs (CC-R or PCR). Studies have shown that carbon cloth enhances anaerobic digestion by accelerating DIET between bacteria and methanogens (Dang et al., 2016b; Lei et al., 2016; Zhao et al., 2015). In order for this to occur, both the electron-donating and electron-accepting species must attach to the surface of the conductive material (Chen et al., 2014; Zhao et al., 2016a). Therefore, bacterial genera attached to carbon cloth and polyester cloth surfaces were compared (Fig. 5). Geobacter species were significantly more abundant on the CC-S (22.97% of the overall community) than PC-S (11.57%). It was not

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surprising that Geobacter were enriched on the carbon cloth as Geobacter have frequently been shown to attach to conductive materials during anaerobic digestion including carbon cloth (Zhao et al., 2017), biochar (Zhao et al., 2016a), and granular activated carbon (GAC) (Lei et al., 2019). However, it was interesting that Geobacter were also significant members of the PC reactor. This is consistent with previous studies that have shown that Geobacter are frequently enriched in anaerobic digesters fed ethanol, even in the absence of conductive materials (Morita et al., 2011; Rotaru et al., 2014b), as it serves as an excellent source of electrons for DIET between Geobacter and Methanothrix or Methanosarcina species (Rotaru et al., 2014a; Rotaru et al., 2014b). Although Geobacter was enriched on both cloth surfaces, it was twice as abundant on the carbon cloth, suggesting that the conductive material further promoted growth of this DIET-capable genus. Clostridium species also dominated the CC-S sample (23.33% overall community abundance), but were barely detectable in the CC-R or any of the PC samples (Fig. 5.). The absence of Clostridium in the PC reactors may have contributed to reactor failure. Further analysis of Clostridium at the species level showed that Clostridium swellfunianum significantly dominated (98.5%) the carbon cloth surface (Fig. S2). C. swellfunianum was isolated from pit mud used for alcohol production (Liu et al., 2014) and was enriched when zero valent iron (ZVI) was used as an extracellular electron donor (Im et al., 2019). Although interspecies electron transfer capabilities of C. swellfunianum have yet to be determined, evidence suggests that some Clostridium species may be capable of DIET. Not only are some Clostridium species able to reduce

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insoluble electron acceptors such as Fe(III) (Dobbin et al., 1999), but they also tend to frequently be enriched in environments supplemented with conductive materials such as carbon felt particles (Xu et al., 2016) and polyaniline nanorods (Qian et al., 2017). The CC and PC cloth surfaces and reactor sludge samples were dominated by archaea in the genera Methanothrix and Methanobacterium (Fig. 6). While Methanothrix were more abundant in CC-S (51.86% of the overall community abundance) and PC-S (58.60%), Methanobacterium were predominantly found in the CC-R (69.02%) and PC-R (48.25%). Both Methanothrix and Methanobacterium species tend to be enriched in anaerobic digesters supplemented with conductive materials (Dang et al., 2016a; Lei et al., 2019; Zhao et al., 2016b). It has been shown that Methanothrix is able to produce methane via DIET with a bacterial partner (i.e. Geobacter) in co-culture studies (Rotaru et al., 2014b), subsurface environments (Holmes et al., 2017), and anaerobic digesters (Liu et al., 2019). Although DIET with Methanobacterium has not been documented, species from this genus can accept electrons directly from metallic iron (Dinh et al., 2004), a cathode (Cheng et al., 2009), and carbon nanotubes (Salvador et al., 2017). Therefore, it is possible that Methanobacterium might also be participating in DIET within the reactor. Further studies into this possibility are warranted. 4. Conclusions Results from this study demonstrated that conductive carbon cloth is an excellent supporting material for AnDMBR treating high-strength brewery wastewater. Maximum organic loads were >50% greater when carbon cloth was used as the

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supporting material compared to polyester cloth. Carbon cloth stimulated significant methane production from complex organic materials, permitted higher organic loading rates, and prevented accumulation of volatile fatty acids. Microbial community analyses revealed that carbon cloth promoted the growth of microorganisms capable of DIET that are known to improve anaerobic digester performance. These results should be taken into consideration in future large-scale attempts to treat high-strength wastewater. Note The authors declare no competing interest.

Appendix A. Supplementary Data E-supplementary data for this work can be found in e-version of this paper online.

Acknowledgments This research was financially supported by the Major Science and Technology Program for Water Pollution Control and Treatment (2017ZX07108-002), the National Natural Science Foundation of China (51708031), and the Beijing Municipal Natural Science Foundation (8184081).

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Figure captions Fig 1. Schematic diagram displaying the submerged AnDMBR systems used in this study. Fig. 2. (A) COD concentrations and COD removal efficiencies and (B) methane production rates in AnDMBRs with carbon cloth or polyester cloth. Fig. 3. Effluent (A) pH, (B) ethanol concentration, and (C) VFAS concentration in AnDMBRs with carbon cloth or polyester cloth. Fig. 4. (A) Transmembrane pressures (TMP) and (B) effluent SS and VSS/TSS ratios over time in the AnDMBRs with carbon cloth or polyester cloth. Fig. 5. Relative abundance of bacterial 16S rRNA gene sequences at the genus level from the carbon cloth and polyester cloth surfaces and reactor sludge. Fig. 6. Relative abundance of archaeal 16S rRNA gene sequences at the genus level

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from the carbon cloth and polyester cloth surfaces and reactor sludge.

Highlights



Carbon cloth as AnDMBR supporting material enhances brewery wastewater treatment



High COD removal efficiency (>98%) was achieved in AnDMBR with carbon cloth



Carbon cloth AnDMBR permits stable operation with 80% higher organic loading

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Species from Methanothrix and Geobacter dominated the microbial community

Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

☐The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

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