Microbial electrosynthesis from CO2: Challenges, opportunities and perspectives in the context of circular bioeconomy

Journal Pre-proofs Review Microbial Electrosynthesis from CO2: Challenges, Opportunities and Perspectives in the Context of Circular Bioeconomy Bin Bian, Suman Bajracharya, Jiajie Xu, Deepak Pant, Pascal E. Saikaly PII: DOI: Reference:

S0960-8524(20)30132-2 https://doi.org/10.1016/j.biortech.2020.122863 BITE 122863

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Bioresource Technology

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29 November 2019 17 January 2020 20 January 2020

Please cite this article as: Bian, B., Bajracharya, S., Xu, J., Pant, D., Saikaly, P.E., Microbial Electrosynthesis from CO2: Challenges, Opportunities and Perspectives in the Context of Circular Bioeconomy, Bioresource Technology (2020), doi: https://doi.org/10.1016/j.biortech.2020.122863

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Microbial Electrosynthesis from CO2: Challenges, Opportunities and Perspectives in the Context of Circular Bioeconomy Bin Biana,┴, Suman Bajracharyaa,┴, Jiajie Xua, Deepak Pantb and Pascal E. Saikalya,* a King

Abdullah University of Science and Technology, Water Desalination and Reuse Center, Biological and Environmental Science and Engineering Division, Thuwal 23955-6900, Saudi Arabia b Flemish

Institute for Technological Research (VITO), Separation and Conversion Technology, Boeretang 200, Mol 2400, Belgium ┴ These

authors contributed equally to this work.

*Correspondence: Pascal E. Saikaly ([email protected]) Abstract Recycling CO2 into organic products through microbial electrosynthesis (MES) is attractive from the perspective of circular bioeconomy. However, several challenges need to be addressed before scaling-up MES systems. In this review, recent advances in electrode materials, microbecatalyzed CO2 reduction and MES energy consumption are discussed in detail. Anode materials are briefly reviewed first, with several strategies proposed to reduce the energy input for electron generation and enhance MES bioeconomy. This was followed by discussions on MES cathode materials and configurations for enhanced chemolithoautotroph growth and CO2 reduction. Various chemolithoautotrophs, effective for CO2 reduction and diverse bioproduct formation, on MES cathode were also discussed. Finally, research efforts on developing cost-effective process for bioproduct extraction from MES are presented. Future perspectives to improve product formation and reduce energy cost are discussed to realize the application of the MES as a chemical production platform in the context of building a circular economy. Keywords

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Microbial electrosynthesis; CO2 reduction; electrode materials; oxygen evolution reaction; circular bioeconomy

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1. Introduction Global warming, mainly due to the greenhouse effect induced by the accumulation of CO2, CH4 and N2O in the atmosphere, is becoming a severe problem (Bajracharya et al., 2017c). CO2 represents the majority of greenhouse gas (GHG) emissions (63% CO2, 24% CH4 and 3% N2O), and main contributor for global warming (ElMekawy et al., 2016). The annual CO2 emission has exhibited a continuous growth trend since 1971, increasing dramatically from 14.1 gigaton to 38.2 gigaton in 2014 (Bajracharya et al., 2017c). In order to restrain the global temperature rise within 2 C according to the Paris Agreement (Peter, 2018) and achieve worldwide carbon balance, effective control of CO2 emissions and gradual reduction of CO2 concentration in the atmosphere have become a priority of research and technological development. Three main strategies have been proposed to combat global warming: (1) reduction of fossil fuel usage (Liu et al., 2015b), (2) development of low-carbon renewable energy source (Granovskii et al., 2007) and (3) CO2 mitigation technologies including carbon capture and storage (CCS) and carbon capture and utilization (CCU) (Bui et al., 2018). So far, consensus has been reached that renewable energy could be utilized to partially replace fossil fuel consumption (Chu et al., 2017). However, developing novel technologies to reduce CO2 concentration in the atmosphere and thus achieve “negative” CO2 emissions is yet a great challenge. Several techniques have emerged for CCU to transform waste CO2 stream into value-added resources, which represents a shift in our perception by considering CO2 as a resource, and hence contributing to circular economy. Unlike CCS which treats CO2 as a waste stream that requires efficient adsorption and storage (Qasem et al., 2018), CCU through catalytic or biological CO2 conversion at large industrial sites is

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now becoming an attractive solution to diverse chemical production in circular carbon economy globally. The thermo/electro catalytic CO2 reduction with mainly metal-based catalysts has been widely studied to convert CO2 into mono-carbon compounds (mostly CO or CH4) (Hou et al., 2006; Kas et al., 2016; Wang et al., 2019). Even though longer-chain hydrocarbons could be generated via CO and/or methanol mediator (Li et al., 2018), the long-term stability of the catalysts and novel techniques for further energy reduction are still under investigation (Wang et al., 2019). To efficiently reduce human dependence on fossil fuels, biological CO2 conversion into value-added chemicals (Savakis & Hellingwerf, 2015; Xu et al., 2019) has been regarded as a cost-effective approach to achieve circular carbon economy. Bioelectrochemical system (BES) has been proposed in the past for waste stream treatment and resource recovery (Katuri et al., 2018). Microbial electrosynthesis (MES) has been specifically designed for cathodic CO2 reduction and diverse product generation by utilizing chemolithoautotrophs as self-sustaining and economic biocatalysts (Bajracharya et al., 2016; Jourdin et al., 2016a). This system does not face the problem of lipid extraction from microalgae cells as in microalgae-based photo-reactors, or unstable catalysts for generating organic products with relatively short carbon-chain from thermo/electro catalytic CO2 reduction. The long-term stability of MES reactors and the high coulombic efficiency of CO2 reduction to products make MES a potentially scalable technology for CO2 utilization in the circular bioeconomy and high-value biofuel generation (Liu et al., 2015a). Currently microbial electrosynthesis of acetate from CO2 has been progressing towards high production (> 10g/L) (Bajracharya et al., 2016; Gildemyn et al., 2015), which is approaching the lower limit of acetic acid concentration in Chinese vinegar (3.5-4.5%)

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(Liu et al., 2004). This indicates the great potential of MES technology for the CO2 transformation into value-added biochemcials in food industry. Apart from acetate, more valuable bioproducts, such as butyrate (Ganigue et al., 2015), caproate (Jourdin et al., 2018) and polyhydroxybutyrate (PHB) (Sciarria et al., 2018), could be generated from CO2 in MES system. The wide diversity of biochemicals generated from CO2 in MES represents another strategical approach for material and chemical synthesis, potentially positioning biotechnology, especially MES, as an effective supplement for circular bioeconomy. In previous studies, different aspects of MES, in terms of reactor configurations, electron transfer mechanism, electroautotrophic microbes and cathode materials utilized in MES have been reviewed in recent years (Table 1). However, several bottlenecks, such as the high energy input, poor CO2 utilization efficiency, and end-product inhibition, are still lacking systematic analysis, which currently restrain the production rates of volatile fatty acids (VFAs) from CO2 at low costs and large scale (Gildemyn et al., 2015). Since energy consumption and product formation rates usually determine the feasibility of biotechnology for scaling up and achieving circular bioeconomy, it is essential to develop cost-effective electrode materials and configurations for reduced energy input, enhanced bacterial colonization, excellent CO2 mass transfer and bioproduct extraction in MES (Bajracharya et al., 2017b; Gildemyn et al., 2015). In this review, we first start with the discussion about the anode materials commonly used in MES. The anode plays a significant role in lowering the energy input for the anodic water splitting. This will be followed by a thorough review of MES cathode materials and configurations for chemolithoautotroph’s growth and various VFAs generation. The impact of direct gaseous CO2 delivery on CO2 mass transfer and pH control at the cathode surface

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is presented in detail. The analysis of energy consumption in MES, including anodic water splitting, cathodic biocatalysis and bioproduct extraction, is discussed. Recommendations for MES system optimization to reduce the overall energy demand and enhance the VFA production are discussed at the end, in the context of translating MES into a viable technology that contributes to circular bioeconomy. 2. Anode modification for efficient electron generation in MES MES for CO2 reduction is an electricity-driven bioproduction process catalyzed by microbes. The reactor configuration usually consists of two main compartments, anode and biocathode chambers, separated with a proton exchange membrane (Fig. 1). Currently most MES studies focus on the cathodic CO2 reduction using various microbial inocula, and different cathode materials and configurations (Aryal et al., 2017a). Cathodic CO2 conversion into acetate has been reported feasible with microbial catalysis at a relatively low cathode potential of ~ -0.4V vs. standard hydrogen electrode (SHE) (Bian et al., 2018a; Nie et al., 2013; Zhang et al., 2013), which represents an overpotential of 110 mV compared to the standard CO2 redox potential (-0.29 V vs. SHE). However, an applied voltage of at least 3 V is usually required to boost the current density and acetate production (Giddings et al., 2015), most of which is believed to bias at the MES anode to drive water splitting (Torella et al., 2015). Oxygen evolution reaction (OER) from water is widely used in MES for proton/electron generation at the anode. OER consumes a large amount of electricity because the reaction is not kinetically favorable, which involves four-electron transfer and is believed to be much more complicated than the hydrogen evolution reaction (HER) at the cathode (Palaniselvam et al., 2017). However, despite its relevance, the development of effective MES anode is

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not gaining attention in MES research. Most MES anodes are made of carbonaceous materials, such as graphite stick (Chen et al., 2016; Nie et al., 2013), graphite plate (Gong et al., 2013), carbon cloth (Bian et al., 2018a) and carbon fiber brush (Alqahtani et al., 2018). However, carbon electrodes exhibits intrinsic electrocatalytic OER activity with an overpotential of more than 600 mV to drive a current density of 5 mA cm-2 (Cheng et al., 2015). To avoid the high energy input and/or reduce the cost of electrode for anodic OER in MES, several strategies have been developed as shown in Fig. 2 such as (1) deposition of small amounts of stable noble catalyst on non-noble electrode for efficient OER; (2) the utilization of photoanodes; (3) the use of anodic reactions other than OER for electron generation; and (4) the use of biotic anode for organic or sulfide oxidation. These strategies are discussed in more detail below. Several metal electrodes, instead of carbonaceous materials, have been utilized as MES anodes to initiate better OER. Ti and Pt metal anodes have been reported to efficiently drive the OER and maintain long-term MES performance without corrosion (Bajracharya et al., 2016; Blanchet et al., 2015). As (noble)-metal electrodes are usually more expensive than carbon, small amount of noble metal catalysts (Ir or Pt) have been deposited onto cheap substrates to serve as MES anodes (Bajracharya et al., 2017b; Bian et al., 2018a). To further reduce the cost for catalyst preparation, biosynthesized reduced graphene oxide doped with transition-metals using electroactive bacteria has been developed for OER with long stability and proposed for potential application in MES (Kalathil et al., 2019). However, since current MES studies mainly focused on the biocathodes with chemolithoautotrophs for CO2 reduction, no results regarding the anodic OER overpotential have been reported

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for these MES anodes with noble metal catalysts, which makes it difficult to identify their long-term stability. Light energy, one of the most abundant renewable resources, can be additionally used at the anode to overcome the overpotential of OER in MES and thus achieving so-called artificial photosynthesis (Fu et al., 2018). Photo-electrochemical (PEC) systems in recent years have been widely reported for hydrogen production through water splitting (Kistler et al., 2019; Yang et al., 2017). To efficiently harvest solar energy, titanium dioxide (TiO2) nanowire arrays have been utilized as photo-absorber and OER catalyst in MES by Liu et al. (Liu et al., 2015a) and Fu et al. (Fu et al., 2018), respectively. An instant photo-response from the MES photoanode induced a current of ~1.2 mA in the absence of external bias, demonstrating the feasibility of minimized energy input for the photo-assisted MES (Fu et al., 2018). Thus it is promising to utilize solar energy in MES for efficient OER and reduced energy input at the same time. Oxygen was reported to be able to diffuse from the anode to the cathode in a twochamber MES reactor (Alqahtani et al., 2019). Previous studies using two-chamber MFCs revealed the negative effects of oxygen diffusion, using ion-exchange membrane, on MFC performance and electricity generation (Suzuki et al., 2016). To reduce the energy input for OER and minimize the negative impacts of oxygen intrusion on chemolithoautotrophic enrichment, chlorine evolution reaction (ClER) could potentially serve as the substitute for OER. The electrochemical formation of chlorine and oxygen gas at the anode occurs according to the following reactions (Bard et al., 1985; Karlsson & Cornell, 2016): 2Cl- → Cl2 + 2e-, E°=1.358V vs. SHE

(1)

2H2O → O2 + 4H+ + 4e-, E°=1.229V vs. SHE

(2) 8

By comparing the standard potentials of reaction (1) and (2), it is obvious that OER requires less activation energy versus ClER. However, high ClER selectivity over OER has been already reported with electrocatalysts, since it is more kinetically favorable with only two electrons involved in chlorine evolution (Karlsson & Cornell, 2016). Finke et al. (Finke et al., 2019) systematically studied the activity of oxygen-evolution and chlorine-evolution through TiO2 electrocatalysts synthesized by atomic layer deposition (ALD). Lower anode overpotential towards ClER induced higher current density (700 mV, ~2 mA/cm2) compared to OER (900 mV, ~0.05 mA/cm2) with the same fluorine-doped tin oxide (FTO) electrode coated at 10 ALD cycles of TiO2. Considering the much lower overpotential to initiate ClER and the huge market size (50-60 million ton/year) of chlorine gas (Gamble, 2019), developing cost-effective anode materials for efficient ClER could be a suitable alternative for OER in MES to achieve circular bioeconomy. Bioanodes are typically used in BESs such as MECs for the removal of chemical oxygen demand (COD) in wastewater with generation of electrons and protons (Katuri et al., 2014). An applied voltage as low as 0.7 V, which is commonly not high enough to drive OER and HER in MES, has been demonstrated to sufficiently drive HER in MEC (Katuri et al., 2014). The main reason for this low voltage is due to the low potential established at the bioanode from the oxidation of organic matter (for example, acetate/HCO3−, E'0 = −0.28 V vs. SHE), instead of the energy-demanding water splitting (H2O/O2, E'0 = 0.82 V vs. SHE). Since MES has been proposed to purify the biogas (mainly CH4 and CO2) from anaerobic digestion (AD) (Jourdin et al., 2016a) and the digested effluent from AD usually contains high strength of persistent organic substances (Ihara et al., 2006), combining bioanodes with biocathodes in MES for AD effluent treatment and biogas upgrading,

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respectively, could enhance the role of AD in circular bioeconomy and help reduce the energy input in MES by replacing the anodic OER reaction (Katuri et al., 2019). The utilization of bioanode has recently been reported in MES reactors with a bipolar membrane (Xiang et al., 2017), however, no details about the anode potential was provided. Another study reported that the bioanode potential could reach as low as -0.2 V vs. SHE to generate electron/proton with higher current density compared with abiotic anode in MES (Tian et al., 2019). Both studies reported a COD removal efficiency of > 45% and a coulombic efficiency of over 60%, demonstrating the feasibility of integrating bioanode in MES systems for both treating wastewater and reducing energy input. Apart from electron generation via organic oxidation at bioanode (Bian et al., 2018b; Sadhukhan et al., 2016), some reduced inorganic compounds (for example, S2-, HS-) could also serve as electron donors through anodic oxidation at lower overpotentials. Sulfide has been converted by microbes to sulfur with electron generation to reduce the anodic overpotential in BESs (Gong et al., 2013; Ni et al., 2019; ter Heijne et al., 2018). The electrochemical oxidation of S2- is shown below (Ni et al., 2019): HS - → S(s) +2e - + H + , Eanode = -0.262V vs. SHE (pH=9; 1M Na+)

(3)

It is obvious that sulfide oxidation is much more thermodynamically favorable than OER and ClER as shown above. Recent studies showed the electron transfer from sulfide to bioanode inoculated with sulfide-oxiding bacteria (SOB) at anode potential of 305 mV (ter Heijne et al., 2018) or 503 mV vs SHE (Ni et al., 2019). Sulfide-driven MES process at 503 mV vs SHE has been successfully demonstrated using SOB-inoculated (Desulfobulbus propionicus and Desulfuromonas) bioanode (Gong et al., 2013). 3. MES cathodes to utilize CO2 as a resource for chemical production

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MES cathode represents the core of MES system as it is the central platform for CO2 recycling and biochemical production. One of the key elements affecting the chemical production from CO2 in MES is the selection of cathode materials because it governs the electroactivity and biocompatibility. Chemically stable cathodes with low cost, high conductivity, high HER capability, and large biocompatible surface area for cell adherence/biofilm formation are preferable for CO2 reduction in MES (Aryal et al., 2017a). The proof of principle for microbial CO2 reduction at the cathode was reported with a graphite stick cathode using Sporomusa ovata as biocatalyst (Nevin et al., 2010). The planar graphite block as a cathode in MES was not able to achieve high acetate production due to its limited surface area for biofilm development. A number of MES cathodes made from carbonaceous, metallic, and carbon-metallic materials have been recently developed in MES. These materials can come in different configurations including planar (such as cloth, plate, and rod) and porous 3D configuration (such as foam and felt). Porous 3D materials with large specific surface area can enhance microbial-electrode interaction and substrate mobility within the electrode even without surface modification (Jourdin et al., 2018). Other configurations such as flow through (Bajracharya et al., 2017d; Jourdin et al., 2018) and gas diffusion cathodes (Alqahtani et al., 2018; Bajracharya et al., 2016) are also beneficial in enhancing CO2 reduction rate in MES. To further enhance the cathodemicrobial interactions, cathode surface modifications have been employed (Bian et al., 2018a; Jourdin et al., 2014; Zhang et al., 2013). An overview of different cathode materials for CO2 reduction in MES is presented in Table 2. Modifications in cathode surface are intended to enhance the electrocatalytic activity and microbial cell adherence to the cathode. For example, carbon cloth electrode after

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modification with chitosan, an amino and hydroxyl-group rich polysaccharide, increased the acetate production rate by 7.6 folds (Zhang et al., 2013). Production of acetate from CO2 reduction was boosted as a result of CO2 adsorption on the porous chitosan, enhanced electron transfer pertaining to biocompatible cathode surface, and better interaction between the positive charges on chitosan and the negative charges on the external surface of bacteria. Besides, carbon nanomaterials have been widely used for the enhancement of conductivity, specific surface area and biocompatibility of MES cathodes. Multi-walled carbon nanotube (MWCNT) coating on reticulated vitreous carbon (RVC) was first utilized to efficiently provide a high specific surface area for bacterial growth and the corresponding acetate production (Jourdin et al., 2014). The high conductivity of the RVCbased cathodes induced by MWCNTs also led to ~100% electron recovery in MES (Jourdin et al., 2015). Modifying the carbon-based electrode with reduced graphene oxide (rGO) also improved the CO2 reduction rates using S. ovata (Chen et al., 2016), enhancing the acetate formation by 11.8 times as compared to the unmodified carbon cloth cathode in MES (Chen et al., 2016). Likewise, metal-carbon complex cathodes were also applied in MES for CO2 reduction. Nickel (Ni) nanowire (Nie et al., 2013), Fe2O3 (Cui et al., 2017) and Fe3O4 (Zhu et al., 2019) were reported to combine with carbonaceous materials as MES cathodes and contribute to the enhanced CO2 reduction rates in MES due to the improved electrocatalytic property of cathode material. A photocathode based on silicon-titanium oxide nanowires (Si-TiO2 NWs) has also been specifically designed to enrich S. ovata cells, which resulted in 4.4 ± 1.0 times higher cell loading compared to the planar Si electrode (Liu et al., 2015a).

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In addition to cathode surface modifications, there is a need to design a better cathode architecture to address the mass transfer limitation in MES (See Table 2). Gas diffusion electrode (GDE) made from activated carbon and Polytetrafluoroethylene (PTFE), VITOCoRE®, was thus employed in MES. The VITO-CoRE® GDE provided a gas–liquid–solid interface for the CO2 diffusion, which improved CO2 mass transfer (Bajracharya et al., 2016). Likewise, a forced flow-through configuration of carbon felt cathodes enhanced the production rates in MES by improving the mass transfer and electrode surface area (Bajracharya et al., 2017d; Jourdin et al., 2018). Remarkably, three layers of non-modified carbon felts as the flow-through cathode at -0.85 V vs SHE produced the highest rate of acetate production at 371±5 g m−2d−1 (Jourdin et al., 2018). This system also produced longer chain organic compounds such as n-butyrate and n-caproate at the rate of 160±29 g m−2d−1 and 46±1 g m−2d−1, respectively. In the latest modification of cathode architecture to address CO2 mass transfer limitation, direct CO2 supply in dual-functional porous Ni-hollow fiber (Ni-HF) membrane cathode was demonstrated to enhance the bioelectrochemical CO2 reduction in MES (Alqahtani et al., 2018; Bian et al., 2018a). Almost 84% of the electrons were recovered as methane via CO2 delivery through Ni-HFs, achieving almost 4 times higher CO2 conversion efficiency compared to CO2 sparging into MES electrolyte (Alqahtani et al., 2018). A follow-up study depositing MWCNT on the surface of Ni-HF further confirmed the superiority of direct CO2 delivery to chemolithoautotrophs on the cathode, with greatly enhanced CO2 adsorption capacity and reduced electron transfer resistance, which led to higher acetate production from CO2 using S. ovata compared to the unmodified Ni-HF (Bian et al., 2018a). The direct CO2 delivery through porous hollow fiber electrodes created

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high CO2 availability at the MES cathode surface, which resulted in higher production of methane and acetate from CO2. CO2 concentration and bubble sizes may also bring variations in the performances of CO2 utilization and bacterial growth in MES. The effect of CO2 concentration, flow rate and bubble size on CO2 fixation was analyzed in tubular microalgae-bioreactors, and the results showed that higher CO2 concentration induced higher cell concentration and photosynthesis productivity (Ryu et al., 2009). The authors also observed higher bacterial growth with smaller CO2 bubble sizes ranging from 31 mm to 61 mm by using smaller pore size (5-10 μm) spargers, which could be attributed to the enhanced gas-liquid interfacial area by reducing the bubble size and thus enhancing mass transfer. The CO2 bubble size could be further reduced using porous membrane electrodes with small pore sizes (< 1 μm), which can lead to better CO2 mass transfer. Not only the CO2 mass transfer and availability will be enhanced, but the local pH at the electrode surface could be adjusted by direct CO2 delivery through the porous membrane cathodes in MES. The pH level in MES utilizing bicarbonate as the carbon source usually increases with time, as protons are consumed to produce VFAs, methane or hydrogen (Ganigue et al., 2015). Acetate production in MES was analyzed with stepwise change in media pH (from 6.7 to 3) and the largest acetate production value was reported at a pH of 5.2 (Jourdin et al., 2016a). It is evident that a slightly acidic environment (pH 5-6) promotes the production of multi-carbon VFAs and inhibit the methane generation at the cathode (LaBelle et al., 2014). Since CO2 sparging into media was reported to be able to create slightly acidic pH (Bajracharya et al., 2016), continuous CO2 sparging along with bicarbonate in media could be an excellent alternative for maintaining pH at 5-6 in MES. Considering all these findings, the future developments

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on cathode architecture in MES could focus more on porous membrane electrodes for direct gas delivery and small bubble production in order to achieve high CO2 concentrations, fast mass transfer and slightly acidic pH at the cathode surface (Katuri et al., 2018). 4. Chemolithoautotrophs at MES biocathodes for CO2 reduction Chemolithoautotrophs can use H2, formate, sulfide and reduced metal ions as electron donors for CO2 reduction through Wood–Ljungdahl (WL), reverse tricarboxylic acid and variants of hydroxypropionate/hydroxybutyrate pathways. Reduced electron donors, especially H2, could be generated through HER at the cathode surface when sufficient reductive potential is imposed under electrochemical settings. In addition, microorganisms may uptake electrons directly from the cathode. Direct uptake of electrons from the cathode has been reported for some species of methanogens (Walker et al., 2019) and sulfate reducing bacteria (Deng et al., 2015). In recent literature, the archaellum of Methanospirillum hungatei was reported to be electrically conductive (Walker et al., 2019), which may facilitate the direct electron transfer from cathode to microbes. Thus, chemolithoautotrophs could efficiently attach to the electrodes for CO2 reduction with the electricity input. Homoacetogens represent a group of taxonomically diverse chemolithoautotrophs that can use CO2 and H2 (electron donor) for anaerobic-autotrophic growth. Several species of homoacetogens from the genus Sporomusa, Moorella, Clostridium have been investigated for CO2 reduction to multi-carbon products in MES (Nevin et al., 2011). Besides pure cultures of homoacetogens, mixed microbial communities are widely employed as biocatalysts in MES. In mixed cultures, the interactions among various microorganisms can result in a final microbiome adapted towards the intended process. The functional shift towards the desired process and the

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adaptive nature of mixed cultures to the operational condition in the reactors make the use of mixed culture communities advantageous for MES applications (Patil et al., 2015; Rabaey & Rozendal, 2010). MES are usually inoculated with i) mixed culture inocula from anaerobic environments (Jourdin et al., 2014); ii) previously enriched inocula from parent MESs (Jourdin et al., 2016a); or iii) selective cultivation of targeted species from mixed culture (Patil et al., 2015). Various sources of mixed culture inoculum used in MES for CO2 reduction are detailed in Table 2. A group of CO2 reducing bacteria from the phylum Firmicutes such as Acetobacterium spp., Acetoanaerobium spp., Trichococcus spp. and Clostridium spp. were predominantly enriched in mixed culture MES biocathodes (Jourdin et al., 2016b; Marshall et al., 2017). High rates of CO2 reduction have been reported at the biocathode of MES, where chain-elongating microbes also became active for the bioelectrochemical conversion of CO2 to medium chain VFA production (Batlle-Vilanova et al., 2017; Vassilev et al., 2018). In recent development in MES research, inocula from hypersaline environments using brine pool sediment and interface electrolyte have been tested for the enrichment of homoacetogens at the cathode (Alqahtani et al., 2019). Genome analysis revealed novel halophilic homoacetogens for CO2 fixation via WL pathway (Alqahtani et al., 2019). The operation of MES system under saline conditions might be advantageous for scaling up as seawater is abundant and can be used as highly conductive electrolyte to reduce ohmic resistance. Selecting a robust and effective CO2 reducing communities from saline environments, that are diverse in microbial composition such as salt marsh, mangrove, and deep sea sediments, can be useful for MES study in this aspect.

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5. Diverse products obtained from CO2 using MES platform In general, acetate is the most common bioproduct generated from CO2 conversion in MES. However, some other products such as butyrate, oxo-butyrate, ethanol, iso-propanol have also been produced as minor products (Ganigue et al., 2015; LaBelle et al., 2014; Nevin et al., 2011). More reduced products were formed as a result of further reduction of the accumulated acetate produced in MES (Sciarria et al., 2018). Production of ethanol from CO2 was reported using S. ovata pure culture when the condition became highly reductive with excess availability of hydrogen (Blanchet et al., 2015). Microbial chain elongation could be thus initiated to produce up to C4-C8 products at the presence of acetate and ethanol (Batlle-Vilanova et al., 2017). The production of longer chain fatty acids from acetate needs ethanol as an electron donor, but in MES under highly reductive condition the cathode or hydrogen also serves as an electron donor for chain elongation (Steinbusch et al., 2011). Ethanol could be produced as an intermediate through the reduction of acetate using hydrogen as depicted in Fig. 3a. Van Eerten-Jansen et al. (Van Eerten-Jansen et al., 2013) first reported the chain elongation of acetate to caproate (C6) using cathode as the electron donor. Acetate and other VFAs produced from CO2 in MES could be the precursor compounds for the bioproduction of other raw chemicals. Production of butyrate (0.16 g L−1 d−1) as the main product from CO2 reduction was reported in MES (Ganigue et al., 2015). Butyrate production rate from CO2 in MES was increased to 0.21 g L−1 d−1 under microbial adaptation (Batlle-Vilanova et al., 2017). Butyrate and caproate production rates reached as high as 160 ± 29 g m-2 d-1 and 46 ± 1 g m-2 d-1, respectively, when the acetate production was as high as 370 g m-2 d-1 in continuous mode using forced flow-through carbon felt

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cathode (Jourdin et al., 2018). Various other VFAs and alcohols have been discovered in MES and production rates have been enhanced with improvements in cathode material and configuration (Table 3). The aforementioned results demonstrate that MES is an attractive approach to supply in-situ electrons or H2 for electrode-driven chain elongation process at the cathode. MES as a production platform becomes attractive in the context of circular economy when the production can be established at high rate, and the end-product can be diversified to special and economically valuable commodities. In CO2 reduction via Wood-Ljungdahl (WL) pathway, acetyl-CoA is a central precursor that may undergo further metabolic conversion to generate various commodity chemicals such as ethanol, butyrate, lactate, 2,3butanediol and butanol under the appropriate conditions (Schiel-Bengelsdorf & Durre, 2012). Solventogenesis metabolism can be introduced into the MES process by changing operational conditions to produce respective alcohols from VFAs (Vassilev et al., 2018). In addition, lactate (C3) and succinate (C4) could also be generated from the intermediate products of CO2 reduction through Krebs cycle (Venkata Mohan et al., 2016). The perspective of production of various value-added products from CO2 by integrating MES with chain elongation mechanism and other bioconversion systems is depicted in Figure 3b. Such perspective presents the MES as the producer of precursory compounds such as H2, CH4 and acetate/short chain fatty acids (SCFA) which can be further upgraded to longer chain carboxylates, biofuels, bioplastics, polysaccharides and protein with multi-step bioconversions (Chu et al., 2019). For example, CH4 produced in MES can be used as a feedstock in syngas platform to produce methanol, formaldehyde, and ethylene (Verbeeck et al., 2018). In case of acetate production in MES along with other SCFAs, further

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upgrading has been reported mainly via chain elongation platform to produce butyrate and caproate as mentioned above (Jourdin et al., 2018). In other approaches of further conversion of SCFAs, production of polyhydroxyalkanoates and single-cell proteins (SCPs) has been reported (Alloul et al., 2018; Molitor et al., 2019). 6. Integrating renewable energy and chain-elongation platform to reduce energy consumption in MES The economics of bioelectrochemical CO2 reduction to different products (formic acid, acetic acid and oxalic acid) in terms of cost-effectiveness, energy and raw material costs has recently been analyzed (ElMekawy et al., 2016). Since acetate is the main product of current MES studies, the discussion on economic analysis is focused mainly on acetate production. In summary, if CO2 is converted to acetate at a rate of 10 g m-2 h-1, one MES stack with a cathode surface area of 45 m2 could reduce 3.94 tons of CO2 and generate 5.37 tons of acetic acid yearly. Considering the electricity cost of 406 EUR/ton of acetic acid generated with 30% electrical efficiency (ElMekawy et al., 2016), the total electricity cost for one MES stack is around 2,180 EUR/year, which is close to the cost for the annual replacement of electrodes and membrane materials (50 EUR/m2). It is worthwhile to mention that the energy cost does not include the energy-intensive processes for acetic acid extraction. To make MES economically viable technology for scale-up, it is necessary to significantly lower the energy consumption required for MES operation and product separation/extraction. As mentioned above, microbial CO2 reduction at the cathode could be achieved by applying a low cathode potential (< -0.4 V vs SHE). Also, cost-effective OER catalysts or photo/bio-assisted anode could be utilized to drive efficient electron generation at the anode

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surface and significantly reduce the energy consumption. Apart from these strategies for reducing energy consumption for MES operation, utilizing renewable energy to replace the traditional electricity input could be another option for future MES scale-up and sustain artificial photosynthesis (Zhang et al., 2013). The increasing abundance and reduced cost of renewable electricity for solar (US$0.04-0.06 kWh–1)approaching parity with fossil fuels, make CO2 transformation via MES increasingly attractive when powered by renewable energy sources (Ross et al., 2019). As the theoretical energy input for one ton of acetic acid production would reach 4.06 MWh with 30% energy efficiency (ElMekawy et al., 2016), the total energy cost would be US$162.4-243.6 if we power MES with solar electricity. This represents a huge decrease from current MES energy cost (406 EUR/ton) for acetic acid production as mentioned above and a great profit margin compared to current market price of acetic acid (~US$625/ton acetic acid) (Christodoulou et al., 2017). Renewable electricity from Photovoltaic (PV) panels is a mature technology to harvest solar energy and can power a separate MES reactor for CO2 reduction (Nevin et al., 2010). A solar-to-chemical efficiency of 10% could be achieved given the assumption of 20% solar-to-electrical conversion efficiency using a commercially available PV panel with an electrical-to-chemical efficiency of 52% (Nichols et al., 2015). Apart from PV panels, photoelectrodes could be applied in MES to further enhance solar harvesting efficiency. Several hybrid photoelectrochemical systems have been reported for solar-driven hydrogen production, followed by CO2 reduction catalyzed by microorganisms/enzymes to produce hydrocarbons (Nichols et al., 2015; Torella et al., 2015). A microbial photoelectrochemical system equipped with black silicon photocathode and bioanodes for hydrogen generation, was recently developed with solely solar energy as power source, achieving a 93-97%

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electron recovery in the form of hydrogen (Lu et al., 2017). To further enhance the solar harvesting efficiency, semiconductors with a narrow bandgap should be developed to enable higher light absorption (Palaniselvam et al., 2017). In addition to the energy input for MES operation, the energy consumption and the material costs are expected to be high for acetate extraction, even if renewable energy is used to power MES (Christodoulou et al., 2017; Gildemyn et al., 2015). In traditional industry, the majority of acetic acid is extracted or purified via distillation, azeotropic distillation and liquid-liquid extraction, which are usually energy intensive and require complex accessories for several equilibrium and reflux stages (Lei et al., 2004). However, due to the nature of MES systems, the media or effluent contains a large amount of salts and suspended biomass, which could be potentially extracted together with acetic acid and contaminate the purification processes. Membrane technology is thus introduced for VFA separation, as well as bacterial control in food and biotechnology industries (Andersen et al., 2016). Membrane electrolysis (Andersen et al., 2016; Gildemyn et al., 2015; Xu et al., 2015) or membrane liquid-liquid (Kucek et al., 2016) extraction have been utilized for in situ extraction of VFAs from anaerobic fermentation and MES. VFAs with different carbon-chain lengths were successfully extracted from the fermentation broth utilizing ionexchange membranes or polymeric hollow fiber membrane modules (Kucek et al., 2016; Xu et al., 2015). Nearly 100% extraction of fermented acetic acid by membrane electrolysis was achieved with a maximum acetic concentration of 80 mM, depicting the possibility of membrane electrolysis in MES application (Andersen et al., 2016). An extraction efficiency of more than 94% with acetic acid concentration as high as 220 mM was achieved by designing a three-chamber MES reactor and integrating an anion exchange membrane

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(AEM) and a cation membrane (CEM) for membrane electrolysis (Gildemyn et al., 2015). However, the increasing salinity of the extraction liquid and the potential fouling of AEM for membrane electrolysis may lead to decreased extraction efficiency for MES operation. Another extraction technique utilizing ion-exchange resin for acetate sorption from MES broth has been also applied (Bajracharya et al., 2017b). Acetate adsorption of 10-20 mg g-1 resin was observed after recirculating the catholyte through the ion-exchange resin. The extraction efficiency was lower compared to membrane electrolysis, probably due to the high affinity between water and acetate molecules, the salt accumulation and biofouling. To reduce the energy cost for extraction and make MES more feasible for industrial CO2 reduction, it is recommended to convert acetate to medium-chain carboxylic acids, which have higher market price, such as caproic acid ($1.6/kg) (Andersen et al., 2015; Khor et al., 2017) and butyric acid (> $3.5/kg) (Baroi et al., 2017), and lower water solubility than acetate. Extraction of medium-chain fatty acids is preferable, since it requires much less energy input (< 2 kWh/m3) compared to acetate extraction (Table 3). The chainelongation from acetate could be conducted either in MES reactors (Batlle-Vilanova et al., 2017; Vassilev et al., 2018) or in separate fermentation reactors after microfiltration of MES effluent. Membrane liquid-liquid extraction unit using hollow fiber membranes pretreated with 6% dodecanol has been recently applied for butyrate extraction from MES reactor (Batlle-Vilanova et al., 2017). Acetate was chain elongated to butyrate, with ethanol serving as electron donors in the MES reactor. An excellent butyrate selectivity (16.4) over acetate was achieved, demonstrating the potential application of chain-elongation technology in MES to reduce the energy cost for VFA extraction. A minimum power consumption of 4.08 ± 0.66 kW h kg-1 product extracted was achieved for the separation of

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medium-chain carboxylic acids after chain elongation using membrane electrolysis, which was far lower compared to the energy input for acetate extraction using the same technique (Xu et al., 2015). Khor et al. (Khor et al., 2017) further lowered the energy consumption for caproic acid extraction (2 kWh kg−1 carboxylic acid extracted) using membrane electrolysis in a fermentation system for the electricity-assisted production of caproic acid from grass. All the results above clearly exhibited the sharp decrease in energy consumption for bioproduct extraction after chain elongation. Hence, such production and extraction system developed out of MES would be relevant in supporting circular bioeconomy. Even though the caproate production rate in MES is yet slower than that in AD through chain-elongation (Jourdin et al., 2018), MES could serve as a complementary technology to AD in the future, if it fully utilizes its anode compartment for wastewater treatment and increases its profitability (Reddy et al., 2018). 7. Future perspectives Transition from the linear model of material and energy production and consumption to a circular bioeconomy is a key aspect in maintaining environmental sustainability for the future. The MES platform could incorporate the use of renewable electricity for CO2 recycling and commodity production, showing a promising prospect for electricity-driven bioproduction of short and medium chain fatty acids from CO2 employing acetogenic bacteria as biocatalysts. MES can further play a complementary role in attaining circular CO2/bio-based economy (Fig. 3c), if we can overcome some limiting factors to its application such as high operating costs and low product specificity as discussed recently by Prévoteau et al. (Prévoteau et al., 2020).

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To bring MES to the level of industrial application, the CO2 conversion rates have to be significantly improved, which could be achieved in three aspects as follows: (1) Ensuring sufficient CO2 availability and electron donors will enhance the enrichment of chemolithoautotrophs. Development of porous membrane electrodes and gas diffusion electrodes in MES systems has been shown to be effective for CO2 delivery to the biofilm (Alqahtani et al., 2018; Bian et al., 2018a). Higher CO2 concentration and smaller CO2 bubbles have been proven to achieve higher mass transfer coefficient, which improved the CO2 utilization efficiency and bacterial growth (Ryu et al., 2009). Therefore, electrically conductive and catalytic porous membrane and gas diffusion electrodes could be utilized to bring MES technology closer to commercialization. However, several operation conditions, such as gaseous CO2 flow rates, bubble size and gas diffusion at the cathode-microbe-media interface, that are believed to greatly enhance the MES performance, should be optimized before introducing this type of cathode architecture into large-scale industrial application. (2) Gaining a better understating of electron transfer mechanisms from the cathode to chemolithoautotrophs is required to develop better strategies for enhancing VFA production rates from CO2 reduction. Direct electron transfer (DET) from the electrode to chemolithoautotrophs appears to be thermodynamically more favorable than indirect electron transfer via the electrochemically evolved hydrogen. However, the coexistence of both electron transfer mechanisms is highly probable in mixed culture biocathodes. Therefore, a clear understanding of the dominant mechanism (i.e., direct versus H2mediated electron transfer) in MES is important for the rational design of cathode. For example, if direct electron transfer is dominant, then biocompatible cathodes with high

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specific surface area are needed for bacterial attachment, whereas for H2-mediated electron transfer, the cathode design can be modified by introducing more active sites for better HER. (3) The selection of highly-efficient chemolithoautotrophs is of high priority. Genetic engineering of appropriate microbes could be one good option. For example, the acetogen Clostridium ljungdahlii was metabolically engineered for the production of more valuable biocommodities (such as butyrate) from H2:CO2 (Ueki et al., 2014). Microorganisms present in saline habitats such as mangrove and salt marsh are excellent habitats for CO2 fixing species and are playing an important role in carbon cycling (Alqahtani et al., 2019). Thus, saline environments could potentially become an ideal location to discover novel and efficient CO2 fixing communities that can potentially produce useful products with diversity in metabolism. The energy cost for MES operation may pose another challenge for scaling-up MES. Several strategies could be adopted to reduce energy input, such as the integration of renewable energy sources to MES, reduction of anodic OER overpotential using low-cost and effective catalyst, utilization of saline electrolyte to reduce ohmic losses, and chain elongation of SCFA to medium chain fatty acids (MCFAs) for easy extraction. Further research on electricity-driven microbial chain elongation is required to develop MCFA production process with high efficiency, reliability and controllability. However, a comprehensive energy analysis should be conducted to identify energy consumption from the different components in MES. Future aspects of improvement in MES from CO2 also include the use of hybrid systems, comprising of autotrophs for CO2 reduction and heterotrophs for further

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conversion of products after CO2 reduction (Fig. 3b). Similarly, hybrids of autotrophs at the biocathode with heterotrophs at the bioanode can be used to achieve energy saving with simultaneous treatment of organic waste streams. Integration of MES with established biotechnologies, such as AD and fermentation, is a promising alternative for future development (Jiang et al., 2019). 8. Conclusion This report summarized the recent development of MES platform for the synthesis of bioproducts from CO2. To lower the energy consumption, comprehensive strategies were proposed for efficient anodic electron generation and bioproduct extraction. Apart from the common requirements of high surface area and excellent bacterial adhesion, MES cathodes with direct CO2 delivery and highly-efficient chemolithoautotrophs were developed to improve the bioproduct formation. The application of MES systems is suggested in the scenario of joint development with renewable energy, wastewater treatment, anaerobic digestion and fermentation, so that a circular bioeconomy of CO2 reduction and diverse chemical production could be achieved. Acknowledgements This work was supported by Competitive Research Grant (URF/ 1/2985-01-01) from KAUST to PS. DP is working on bacterial conversion of CO2 and hydrogen into fuels in the project BAC-TO-FUEL funded by the European Union's Horizon 2020 Research and Innovation Program under Grant Agreement no. 825999. References 1. Alloul, A., Ganigué, R., Spiller, M., Meerburg, F., Cagnetta, C., Rabaey, K., Vlaeminck, S.E. 2018. Capture–Ferment–Upgrade: A Three-Step Approach for the Valorization of

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Figure and Table Captions

Fig. 1. Schematic of a microbial electrosynthesis (MES) cell powered with different energy sources. PEM: proton exchange membrane. Reproduced with permission (Katuri et al., 2018). Copyright 2018, John Wiley & Sons, Inc. Fig. 2. A scheme of different anode strategies in MES for reducing energy input. All the values included in this scheme are based on the standard redox potential (vs. SHE) of the different anodic reactions for electron generation. a -0.28 V vs SHE represents the oxidation potential of acetate, which is a common organic compound present in wastewater. Fig. 3. (a) A scheme of direct CO2 delivery through the pores on hollow fiber membrane electrode for the generation of diverse bioproducts from CO2 with different microbes. (b) The prospect of producing high-value products in MES from CO2 by further bioprocessing of primary products. (PHB: Poly-hydroxybutyrate, PHA: Poly-hydroxyalkanoates) (c) MES platform for biochemical/biofuel production and methane upgrading through integration with other bioprocesses. Table 1 A summary of recent reviews that have appeared on different aspects of MES. Table 2 Overview of cathode materials, products and production rates in microbial electrosynthesis from CO2. Table 3 Materials and energy input for VFA extraction via (bio)-electrochemical systems.

44

Fig. 1. Schematic of a microbial electrosynthesis (MES) cell. PEM: proton exchange membrane. Reproduced with permission (Katuri et al., 2018). Copyright 2018, John Wiley & Sons, Inc.

45

Fig. 2. A scheme of different anode strategies in MES to reduce energy input. All the values included in this scheme are based on the standard redox potential (vs. SHE) of the different anodic reactions for electron generation. a -0.28 V vs SHE represents the oxidation potential of acetate, which is a common organic compound present in wastewater.

46

Fig. 3. (a) A scheme of direct CO2 delivery through the pores on hollow fiber membrane electrode for the generation of diverse bioproducts from CO2 with different microbes. (b) The prospect of producing high-value products in MES from CO2 by further bioprocessing of primary products. (PHB: Poly-hydroxybutyrate, PHA: Poly-hydroxyalkanoates) (c) MES platform for biochemical/biofuel production and methane upgrading through integration with other bioprocesses.

47

Table 1 A summary of the recent reviews that have appeared on different aspects of MES. Review (Rabaey & Rozendal, 2010) (Lovley & Nevin, 2013) (Tremblay & Zhang, 2015) (Roy et al., 2016) (May et al., 2016) (Aryal et al., 2017a) (Bajracharya et al., 2017a) (Aryal et al., 2018a) (Jiang et al., 2019) (Chiranjeevi et al., 2019) (LaBelle et al., 2019) (Bajracharya et al., 2019) (Bakonyi et al., 2020) (Prévoteau et al., 2020)

Focus point One of the first reviews explaining the overall concept of MES and other biocathodic production processes The concept of electrobiocommodities produced directly via electrode-tomicrobe electron transfer or indirectly with electrochemically generated electron donors such as H2 or formate was described A detailed description of electroautotrophic microbes that utilize electricity as electron source for CO2 reduction A review describing different bioreactor designs for MES An interesting perspective on extracellular transfer of electrons to acetogenic microorganisms in MES An overview of cathode materials for MES from carbon dioxide The most recent advances in biocatalysts development and process design in bioelectrochemical systems for CO2 transformations were reviewed A detailed review on utilizing MES for biogas upgrading A quantitative analysis of the state-of-the-art on MES and its comparison with electro-fermentation concept A state-of-the-art report on enzymatic electrochemical CO2 reduction for chemical production A detailed account of acetate producing biocathode from the research team at University of South Carolina A comprehensive overview of bioelectrosynthesis based on microbes (MES) and enzymes (enzymatic electrosynthesis) An evaluation of membrane-based technologies for effective separation of CO2 and biohydrogen and subsequent conversion of CO2 using MES A critical overview of a decade of research on MES from CO2

48

Table 2 Overview of cathode materials, products and production rates in microbial electrosynthesis from CO2. Type of cathode

Cathode materials

Microbial inoculum

Cathode potential (V vs SHE)

Current density § (Am-2)

Unmodified Carbon based cathode

Graphite granules

Enriched brewery WW sludge S. ovata

-0.59 -0.68

-0.8 (kA m3) -0.25±0.06

Gas diffusion cathode VITO-CoRE RVC foam (Continuous mode) 3 Carbon felts stacked together (flow through, continuous)

Enriched Anaerobic sludge Enriched acetogenic culture Enriched mixed culture

-1

3 Carbon felts stacked together, flow through, continuous, at high rate CO2 feed CC-SS-AC CC-SS CC

Enriched mixed culture

Modified carbon cathodes

Acetate production rate (gm-2d-1) 1.03£

CE in acetate (%)

Other VFAs and alcohols (gm-2d-1)

Reference

69

-

2.25

79±6

-

-20

36.6

35±8

nC4 & EtOH

-1.1 to -1.3

-83.3

196.8

35

-

-0.85

-110±20

371± 5

nC4 (160±29), nC6 (46± 1) VFAs

-1.02

-126

234±57.7

91±9 (all organic s) 29±6.8

(Marshall et al., 2013) (Giddings et al., 2015) (Bajracharya et al., 2016) (LaBelle & May, 2017) (Jourdin et al., 2018)

-0.9

-100.8

157±25.6

24±4.9

Enriched mixed culture

-0.6

-6 mA -2.3 mA -2 mA

1.7£ 1.7£ 1.4£

47 44 40

Carbon felt (with 5 g L-1 EtOH in media) Chitosan on Carbon cloth

Raw + acclimated activated sludge S. ovata

~ -0.95

-10

-

-0.4

-0.47

3D RVC with MWCNT

Enriched mixed culture Enriched mixed culture

-0.85 -1.1

Graphite disk

MWCNT-RVC

nC4 (125±45), nC6 (42±10) VFAs nC4 (106±6), nC6 (64±3) VFAs nC4 VFA & EtOH

(Jourdin et al., 2019)

nC6 (2.1 ± 0.01£) VFA -

(Jiang et al., 2020)

13.5±3.3

80.3 ± 0.5 86 ± 12

-102

685±30

100±4

-

(Jourdin et al., 2015)

-200

1330

84±2

-

(Jourdin et al., 2016a)

(Jourdin et al., 2019) (Modestra & Mohan, 2019)

(Zhang et al., 2013)

49

CC-rGO-TEPA

Modified with metal/metal oxide

3D-Graphene carbon felt composite Graphene Paper CC coated with PEDOT:PSS MXene Ti3C2Tx-coated carbon felt electrode Graphite Stick -Ni Nano wire Si-TiO2 nanowire photocathode 3D Iron oxide modified carbon felt 3D Graphene Ni-foam Porous Ni-hollow fiber with MWCNTs NiMo deposition on doped Si wafer NiMo deposition on doped Si wafer

S. ovata adapted on Methanol S. ovata

-0.69

-0.23

62.4±26.6

83 ±3

-

(Chen et al., 2016)

-0.69

-2.4

54.6± 1.7

86 ± 3

-

(Aryal et al., 2016)

S. ovata S. ovata

-0.69 -0.69

-2.5 -3.2

39.8 59.5

90.7 87.2

-

(Aryal et al., 2017b) (Aryal et al., 2018b)

Mixed culture from WWTP sludge S. ovata

-0.6

-0.1742

12.24†

41

C3 (13.95†), nC4 (25.08†) VFA

(Tahir et al., 2020)

-0.4

-0.63

3.4

82 ± 14

-

(Nie et al., 2013)

S. ovata

-0.595

-3.5

ng

86 ± 9

-

(Liu et al., 2015a)

S. ovata

-0.69

ng

25.4 *

86 ± 9

-

(Cui et al., 2017)

Mix culture from MFC

-0.85

-10.2

~ 0.15* £

70

(Vassilev et al., 2018)

S. ovata

-0.4

-0.33

1.85

83±8

nC4, i-C4, nC6 VFAs and their alcohols -

S. ovata

-0.7

-10

6.7†

95-100

-

(Kracke et al., 2019)

A. woodii

-0.7

-10

6†

~100

-

(Kracke et al., 2019)

(Bian et al., 2018a)

surface area based current densities, £ unit in g L-1 d-1, * calculated from the provided graphs of the products, † calculated from g L-1 d-1 value. CECoulombic efficiency, VFAs-Volatile fatty acids; ng-not given, 3D-Three dimensional, RVC-reticulated vitreous carbon, CC-Carbon cloth; SS-Stainless steel; ACActivated carbon; WWTP-Wastewater treatment plant; EtOH-Ethanol; VFA C3 -propionate, nC4-n-Butyrate; i-C4-isobutyrate; nC6-n-Caproate; MWCNT-Multiwalled Carbon nanotube, rGO-reduced graphene oxide, TEPA-tetraethylene pentamine, PEDOT:PSS-poly(3,4-ethylenedioxythiophene):polystyrene sulfonate polymer § Projected

50

Table 3 Materials and energy input for VFA extraction via (bio)-electrochemical systems. Cathode

Membrane

Product

Carbon felt Carbon felt

CEM & AEM CEM & AEM CEM BPM AEM 10 bipolar 10 AEM 1 CEM AEM AEM & CEM

Acetate Acetate Acetate Acetate Acetate Succinic acid

Graphite felt 316 SS

316L SS Ti mesh Pt coated Ti plate SS felt SS mesh

10 AEM & CEM AEM AEM

Energy input for Reference a -1 extraction (kWh kg ) 19 (Gildemyn et al., 2015) 26.5 (Gildemyn et al., 2017) 44.3 30.7 ~30.5 (Baek et al., 2018) 6.3 (Prochaska et al., 2018)

C2-C6 Acetate, Butyrate Propionate VFAs

2 5.43

(Andersen et al., 2015) (Pan et al., 2018)

0.395

(Bak et al., 2019)

Caproic acid n-Caproic/caprylic acid

2 4.08 ± 0.66

(Khor et al., 2017) (Xu et al., 2015)

a

Calculated based on the energy consumption per kg of the product extracted from bioreactors. CEM - cation exchange membrane, AEM - anion exchange membrane, AC - activated carbon, BPM - bipolar membrane.

Author Contributions Section

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B.B and S.B contributed equally to this work. All authors contributed in writing the article and in reviewing and editing the manuscript before submission. B.B prepared the graphical abstract and Figures 2, 3 and 5. S.B prepared Figure 4.

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:

 MES

cathode for better bacterial growth and CO2 delivery are reviewed

 Strategies

are provided for energy-efficient anodic electron generation

 MES

chain-elongation suitable for high-value product formation and extraction

 MES

integrated with other bioprocesses can be promising to sustain circular economy

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