Biotechnology Advances 64 (2023) 108123 Contents lists available at ScienceDirect Biotechnology Advances journal homepage: www.elsevier.com/locate/biotechadv Research review paper Industrial bioelectrochemistry for waste valorization: State of the art and challenges Diego Maureira a, Oscar Romero b, *, Andrés Illanes a, Lorena Wilson a, Carminna Ottone a, * a School of Biochemical Engineering, Pontificia Universidad Católica de Valparaíso, Avenida Brasil 2085, Valparaíso, Chile b Bioprocess Engineering and Applied Biocatalysis Group, Departament of Chemical, Biological and Enviromental Engineering, Universitat Autònoma de Barcelona, 08193, Spain A R T I C L E I N F O A B S T R A C T Keywords: Bioelectrochemistry has gained importance in recent years for some of its applications on waste valorization, Bioelectrochemical systems such as wastewater treatment and carbon dioxide conversion, among others. Carbon dioxide reduction The aim of this review is to provide an updated overview of the applications of bioelectrochemical systems Enzymes (BESs) for waste valorization in the industry, identifying current limitations and future perspectives of this Electrodes materials technology. BESs are classified according to biorefinery concepts into three different categories: (i) waste to Microbial fuel cell Wastewater treatment power, (ii) waste to fuel and (iii) waste to chemicals. Carbon-based materials The main issues related to the scalability of bioelectrochemical systems are discussed, such as electrode construction, the addition of redox mediators and the design parameters of the cells. Among the existing BESs, microbial fuel cells (MFCs) and microbial electrolysis cells (MECs) stand out as the more advanced technologies in terms of implementation and R&D investment. However, there has been little transfer of such achievements to enzymatic electrochemical systems. It is necessary that enzymatic systems learn from the knowledge reached with MFC and MEC to accelerate their development to achieve competitiveness in the short term. techniques and applications of bioelectrochemistry systems see Barlett 1. Introduction (2008). Bioelectrochemical systems (BESs) have attracted much attention Bioelectrochemistry, which combined electrochemical and among researchers because they offer the advantage of combining the biochemical processes, has attracted much attention in the last ten years treatment of waste effluent with the simultaneous production of a due to the contribution in terms of catalytic properties that biological valuable product (Zheng et al., 2020). BESs are able to harness the en­ agents (enzymes or living cells) can make to meet the sustainability and ergy remaining in waste, which would otherwise be thrown away. Thus, circular economy principles (de Fouchécour et al., 2022; Al-Sahari et al., BES technologies can be classified, according to the biorefinery con­ 2021; Zhang et al., 2022; Chandrasekhar et al., 2021; Cai et al., 2022). cepts, in waste to power (WtP), waste to fuel (WtF) and waste to The combination of biological systems with electrochemical cells is chemicals (WtC). WtP, WtF and WtC have become popular terms within possible due to the fact that a key part of biological systems are involved the valorization of wastes, where the scope is to produce electric energy, in fundamental processes of energy use and capture (Barlett, 2008). For fuels and organic compounds of commercial interest, respectively, by instance, redox reactions in microorganisms are involved in the oxida­ using waste as raw material. tion of carbon substrates to CO2 with the concomitant generation of In this context, wastewater, agro-industrial wastes and greenhouse energy molecules such as ATP; in the case of plants, solar energy is gases, such as CO2, are the main residues studied with BES technologies. transformed into ATP molecules by means of cascade redox reactions. In Carbon dioxide is one of the main greenhouse gases, its anthropogenic both cases, there is a flow of electrons through an electron transport generation being the main cause of the increase in concentration in the chain, which involves a series of redox proteins and enzymes in a atmosphere. Carbon dioxide reduction is one of the major goals of the constantly fluctuating state of oxidation and reduction. The application climate change battle and finding new alternatives is essential. Among of an external voltage has been proven to yield to a certain degree of the 17 sustainable development goals proposed by the United Nations, manipulation of cellular metabolism. For fundamentals, experimental the capture and recycle of CO2 is part of objective number 13: “Take * Corresponding authors. E-mail addresses: oscarenrique.romero@uab.cat (O. Romero), carminna.ottone@pucv.cl (C. Ottone). https://doi.org/10.1016/j.biotechadv.2023.108123 Received 16 June 2022; Received in revised form 24 February 2023; Accepted 26 February 2023 Available online 2 March 2023 0734-9750/© 2023 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Nomenclature MFC Microbial fuel cell MOF Metal organic frameworks ABTS 2,2′ -azino-bis(3-ethylbenzo- thazoline-6-sulphonc acid) MV Methyl viologen ADMI American Dye Manufacturer’s Institute NA Naphthoquinone AEM Anion exchange membrane NADþ Nicotinamide adenine dinucleotide AC Anodic chamber NADH Nicotinamide adenine dinucleotide (reduced form of AQDS Anthraquinone-1,6-disulfonic acid NAD+) ATP Adenosín trifosfato NER Net energy recovery BE Benzoquinone NPV Net present value BeC Bioelectrolytic cell NR Neutral red BES Bioelectrochemical system OLR Organic loading rate BesC Bioelectrosynthesis cell Ox Oxidized species BFC Biofuel cell Pd Power density BOD Biochemical oxygen demand PEM Polymer exchange membrane CC Cathodic chamber PEMFC Proton exchange membrane fuel cell CE Counter electrode PHA polyhydroxyalkanoate Ceff Coulombic efficiency PHB poly (3-hydroxybutyrate) CEM Cation exchange membrane, PMS Phenazine methosulfate CO Cobaltocene RE Reference electrode COD Chemical oxygen demand Re Reynolds rotation number DET Direct electron transfer Red Reduced species E Potential difference RI Riboflavin EEC Enzymatic electrochemical cell RM Redox mediator EES Electroenzymatic synthesis SHE Standard hydrogen electrode EFC Enzymatic fuel cell SPI Specific power input f Flow rate STS Stirrer tip speed FDH Formate dehydrogenase TLR Technology readiness levels HRT Hydraulic retention time UASB Upflow anaerobic sludge blanket. I Current V-Nase Vanadium nitrogenase i Current density VTR Volumetric treatment rate IEM Ion exchange menbrane WAS Waste activated sludge LCA Life cycle assessment WE Working electrode MB Methylene blue WIPO World Intellectual property organization MEC Microbial electrolysis cell WtC Waste to chemical MES Microbial electrochemical synthesis WtF Waste to fuel MET Mediated electron transfer WtP Waste to power urgent action to combat climate change and its impacts”. in the literature and is responsible to open opportunities for the devel­ Around 380,000 million m3/year of wastewater (equivalent to 152 opment of novel applications of BES, like bioelectrolytic cells (BeC), and million of Olympic swimming pools) are produced worldwide, and this most recently bioelectrosynthesis cells (BesC), among others not value is expected to increase by ca. 2% annually (Qadir et al., 2020). considered in this review. Although efforts in the scientific community Furthermore, according to a study performed by the European Com­ have been focused on the development of BESs for the conversion of mission, the treatment of wastewater that each individual produces wastewater and CO2 into valuable products, their scalability to indus­ leads to 17 kg/year of dry sludge (European Commission, 2017). Thus, it trial level remains a challenge. represents a huge problem for big cities due to the high volumes of The first pilot-scale MFC system reported was a modular reactor with wastewater that need to be treated and the high amounts of sludge that a volume of 1 m3 using brewery wastewater as feedstock (Waller and need to be discarded or processed annually. Some strategies for recov­ Trabold, 2013). After almost a decade, there are a few companies of­ ering bioactive compounds from sludge have been proposed (Cristina fering MFC or MEC solutions for wastewater treatment (Jadhav et al., et al., 2020); however, they are not sufficient to considerably reduce the 2022). However, there is still no consensus in the literature about the amount of waste that needs to be discarded. The current treatment of criteria that need to be taken into consideration for the scale-up of BES wastewater leads to a high energy expenditure, mainly related to the reactors. This work aims to provide an updated overview of the appli­ high requirements of aeration for the activated sludge process, which cations of BESs for waste valorization in the industry to identify current represents 50% of the energy requirement of the plant (Liu and Tay, limitations and future perspectives of the technology. In order to fulfill 2001). The aerobic consortia require constant aeration since it is at this this objective, this review will be divided in four sections: 1. BESs, where stage where most of the organic matter present in the wastewater stream the main parts involved in a bioelectrochemical cell and the mechanism is degraded. Paradoxically, the energy potential present in municipal of action will be described; 2. Bioelectrochemical approaches for waste wastewater ranges from 1.16 to 3.09 kWh/m3 (Alsayed et al., 2020); valorization, discussing the wastes used as substrate and the respective thus, finding alternatives to recover this stored energy is crucial to meet commercially valuable products; 3. Consideration related to the scale-up the aspirations of a sustainable society. of BES, where the main variables to take into account when scaling up In the last decade, an increasing number of scientific articles related BES to a commercial level will be described; 4. Projection of BES tech­ to the development of BESs have been published, as shown in Fig. 1. The nologies; this final section will give a perspective of BES as a viable greatest number of publications are related to biofuel cells, and in commercial alternative to apply in waste valorization. particular, microbial fuel cells (MFC), which was the first BES proposed 2 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Fig. 1. Evolution of the number of scientific articles related to bioelectrochemical systems in the last decade, divided as biofuel cells (BFCs), bioelectrolytic cells (BeCs) and bioelectrosynthesys cells (BesC). (Source: Scopus, December 2022). 2. Bioelectrochemical systems (BESs) however, crucial advances in protein engineering have allowed signifi­ cant progress in enzyme biocatalysis and its implementation on an in­ BESs involve the use of microorganisms or enzymes with an elec­ dustrial scale of production for different products, even from non- trochemical system to exert influence over the metabolism by affecting conventional substrates (Sakkos et al., 2019). the oxidation and reduction ratios. BESs are unique systems capable of In BES, electron transfer can be divided into two mechanisms: direct converting the chemical energy of organic matter into electricity, or mediated, as depicted in Fig. 3. In the direct electron transfer (DET) hydrogen or chemical products. In Fig. 2 a typical two-chamber bio­ mechanism, the enzymes or microorganisms are directly wired to the electrochemical cell configuration is depicted, with an ion exchange electrode. In the case of enzymes, the DET of electrons occurs for dis­ membrane in the middle as separator. At laboratory scale, the electro­ tances between the electrode surface and the redox center of the enzyme chemical cell is made up of a working electrode (WE), a counter elec­ below 1.4 nm (Kumar et al., 2017). The DET mechanism in microor­ trode (CE) and a reference electrode (RE). The reaction of interest takes ganisms occurs when either the microorganism has conductive pili, or place at the WE. The CE allows to close the circuit and the flowing of conductive materials/proteins are present in their outer membrane charges. RE serves for measuring the potential of a single chamber. (Lovley, 2017; Mohan et al., 2014). As an example, Geobacter and She­ If the reaction is spontaneous in nature, the flow of electrons will wanella are electroactive bacteria in the group of microorganisms with allow the generation of energy; in this case, the electrochemical cell is a reported DET capabilities (Creasey et al., 2018; Doyle and Marsili, 2018; galvanic cell. If the reaction is not thermodynamically favorable, the Hirose et al., 2019; Lovley, 2011; Lovley and Walker, 2019). energy needs to be applied from an external source to force the reaction; The mediated electron transfer (MET) mechanism involves the use of in this case, the cell is an electrolytic cell (Bajracharya et al., 2017). redox mediators (RMs). RMs act as intermediate electron carriers be­ BESs make use of an electrochemical cell coupled to a biological tween the biological agent and the electrode surface allowing to obtain catalyst to develop the reaction of interest, where the catalyst is either the final redox reaction at the electrode surface. The possibility exists coupled to the cathodic or to the anodic chamber, depending on whether that the RMs do not establish a direct interaction with the catalyst to the reaction of interest is a reduction or an oxidation. In the case of generate electron transfer, but interact with a third partner, such as a wastewater treatment, the biological catalyst is located in the anodic cofactor; this is called biological transfer of RMs and cofactor. A vast chamber to oxidize the organic matter, as it occurs in microbial fuel cells literature could be founded with respect to the use of redox mediators in (MFCs) or in microbial electrolysis cells (MECs). In the case of CO2 the electrochemical regeneration of NADH (Gajdzik et al., 2012). Also, it conversion, the biological catalyst is located in the cathodic chamber in has been observed that some microorganisms can secrete redox media­ order to carry out its reduction (BesC). tors; for example, a phenazine-based mediator has been found on MFC Although most of the existing literature focuses on the use of mi­ inoculated with Pseudomonas sp. (Pham et al., 2008). croorganisms for the valorization of waste products, the use of enzymes RM are often used in BES to enhance the electron transfer from mi­ has gained relevance in recent times (Cocuzza et al., 2022; Ottone et al., croorganisms or enzymes to the working electrode and can be of natural 2021a). The use of isolated enzymes presents clear-cut advantages to or artificial origin. Their uses in electrochemistry are based on their whole-cell systems, such as better control of reaction parameters and capacity to accept (reduce) and give (oxidize) electrons to other species reaction monitoring, and avoidance of unwanted side reactions, leading (Martinez and Alvarez, 2018). A thorough discussion of redox mediators to higher production yields (Petroll et al., 2019). Besides, the behavior in will be presented in the following sections. terms of reaction kinetics of the enzymatic BES is quite similar to chemical catalysts. However, in microbial systems the metabolic path­ ways and the synthesis of secondary metabolites need to be considered; 3 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Fig. 2. Schematic representation of a bioelectrochemical cell applied for waste valorization with the production of energy, hydrogen or organic compounds. IEM: Ion-exchange membrane. The reduced (red) and oxidized species (ox) in each chamber will depend on the bioelectrochemical system (BES) as indicated. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) Fig. 3. Schematic representation of different mechanisms of electron transfer from electrode to redox species. 4 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 3. Bioelectrochemical approaches for waste valorization alternatives that have been proposed to reduce the overpotential, bio­ cathodes have been highlighted as the most suitable for being cheap and This section gives a brief description of the different BES according to easy to operate (Izadi et al., 2019; Mohamed et al., 2020; Samrat et al., the classification of the biorefinery concepts WtP, WtF and WtC. A 2018; Sindhuja et al., 2018). schematic diagram of the products and the systems involved is shown in In MFCs, an electric current flows through the anode chamber into Fig. 4. the cathode chamber producing electricity by energy conversion from In terms of the different substrates used in BES, the wastewater from the breakdown of chemical bonds in the organic matter (Waller and agribusiness has great potential since it has a high organic load Trabold, 2013). MFC cannot produce the same level of voltage and (chemical oxygen demand (COD) > 1 g/L) and a high degree of biode­ current density obtained in classical chemical fuel cells (Muddemann gradability (biochemical oxygen demand (BOD)/COD>60%) (Callegari et al., 2019). et al., 2018). Therefore, these waste streams are highly attractive to be Analogous to MFC, enzymatic fuel cells (EFC) produce electric cur­ used in an MFC system. It should be noted that despite the development rent by the catalytic oxidation of a fuel. Nevertheless, in contrast to MFC, of current domestic wastewater treatment technologies, they are highly the exploitation of waste as a substrate for EFC is still an emerging energy-demanding due to the need to stabilize this type of waste, so research field. Wastewater containing organic compounds could be alternatives that allow energy reduction are extremely attractive. potentially used as fuel for EFCs. For instance, alcohol dehydrogenase (Galindo-de-la-Rosa et al., 2018, 2020; Tomassetti et al., 2020) or glucose oxidase (Bahar and Yazici, 2018; Chung et al., 2018; del Torno- 3.1. Waste to Power with a biofuel cell (BfC) de Román et al., 2018) modified anodes have been studied using alcohol and glucose solutions, respectively. However, having waste valorization The use of a biological agents, such as bacteria or enzymes, to pro­ in mind, it is necessary to study the interactions that other molecules duce energy in the form of electricity by means of an electrochemical present in the waste may have with the electrochemical system. In cell is known as biofuel cells (BfCs). Microbial fuel cells (MFCs) are addition, the high selectivity of enzymes works against the system, as characterized by having the electroactive bacteria communities in the they cannot efficiently utilize complex waste streams containing anode. The microorganisms consume the substrate from the media, different organic compounds. growing and forming films on the electrode. Looking for further cell improvements, some researchers have proposed the use of biotic cath­ odes as well, as an alternative to overcome the limitation regarding oxygen as the ultimate electron acceptor. Among the different Fig. 4. Diagram of the products reported in the literature for the valorization of waste using a bioelectrochemical system technology. MEC: microbial electrolysis cell, EEC: enzymatic electrochemical cell, BeC: bioelectrolytic cell, EFC: enzymatic fuel cell, MFC: microbial fuel cell, BFC: biofuel cell, EES: electroenzymatic synthesis, MES: microbial electrochemical synthesis and BesC: bioelectrosynthesis cell. 5 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 3.2. Waste to Fuel with a bioelectrolytic cell (BeC) acceleration of the NAD+/NADH redox cycle, which facilitates glyco­ lytic metabolism and, in turn, PHB production. Other substrates, such as Hydrogen (H2) is recognized as one of the cleanest energy carriers, oily coffee waste, have been tested for PHB production by fermentation having a much higher gravimetric energy density than fossil fuels (Jia with Ralstonia eutropha (Bhatia et al., 2018), which illustrates the great et al., 2020). So far, its production comes mainly from the use of fossil potential of BES and the opportunities for waste treatment with the fuels (e.g Hydrocarbon catalytic reforming or coal gasification), which simultaneous production of valuable products. leads to huge emissions of CO2 (Cormos et al., 2018). Regarding the enzymatic reduction of CO2, formate dehydrogenase An alternative environmentally-friendly technology for producing (FDH) and vanadium nitrogenase (V-Nase) have been studied as cata­ H2 is the microbial electrolysis cell (MEC). While MFCs produce energy lysts for the one-step production of formic acid and methane, respec­ by organic matter oxidation, MEC requires an output source of energy to tively (Kuk et al., 2019; Álvarez et al., 2017; Grasemann and Laurenczy, partially reverse the process to generate H2 from organic matter 2012; Su et al., 2016; Pietricola et al., 2020; Pietricola et al., 2021). Also, (Chorbadzhiyska et al., 2011). H2 is obtained at the cathode by the a cascade multienzyme system has been considered to produce methanol reduction of the protons produced by the degradation of organic matter starting from CO2 (Liu et al., 2020a; Ren et al., 2020; Zhang et al., 2021). at the anode (see Fig. 2). Usually, an ion exchange membrane separates In the reduction of CO2 to formic acid with FDH, the nicotinamide the anodic and cathodic chambers allowing only the passage of protons. dinucleotide (NAD) acts as RM, which is regenerated in the electro­ The use of the membrane has the advantage of producing H2 with higher chemical cell (see Fig. 3). The regeneration of the cofactor is a key step purity than obtained in the counterpart with only one chamber (Kadier for the integration of enzymes and electrochemistry, since its high cost et al., 2016). The voltage required for the reaction of H2 production makes regeneration mandatory for successful industrial implementation varies between 0.2 and 0.8 V, which is much lower than in a non- (Ottone et al., 2021b; Pietricola et al., 2022). biological water electrolysis cell, which requires voltages between The electric wiring of nitrogenases differs from that the one for FDH 1.23 and 1.8 V (Kadier et al., 2016). MECs have been used with a range since nitrogenases are ATP-depending enzymes. Although nitrogenases of substrates similar to those already described for MFC, including need ATP as a cofactor, the immobilization of the catalytic subunit of the wastewater. The organic matter removal from wastewater using MEC enzyme on electrodes makes the cofactor dispensable with the conse­ ranges between 60 and 90%, similar to that obtained with a MFC quent economic benefits making the use of nitrogenase-based systems (Escapa et al., 2012; Hussain et al., 2018; Liu et al., 2012). more feasible for large-scale applications. Nitrogenase is made of two In an enzymatic electrolysis cell (EEC), hydrogenases containing the main components, a Fe-protein and a bimetal-protein ([Fe-V] or [Fe- [Ni-Fe] and [Fe-Fe] groups can catalyze the hydrogen reaction in the Fe]). In the Fe-protein ATP is hydrolyzed to start the reduction cathode with similar oxidation rates than in a platinum electrode cascade reaction which ends up on the [Fe-V] cofactor with the CO2 (Chenevier et al., 2013; Jones et al., 2002; Vignais et al., 2001). The reduction to CH4 (Hu et al., 2018). In the EES systems, the coupling of differences between the two groups, [Ni-Fe] and [Fe-Fe], are the cata­ the [Fe-V] or [Fe-Fe]-protein unit is done directly to the cathode, leading lytic properties and the stability at aerobic conditions. The [Fe-Fe] group to a direct transfer of the electrons from the catalytic center of the exhibits better catalytic properties than the [Ni-Fe] group (Bandyo­ enzyme to the cathode during the reaction of reduction of CO2 to CH4 padhyay et al., 2010), but the first one is strongly sensitive to oxygen (Lu (Milton and Minteer, 2019). and Koo, 2019). In general, [Ni-Fe]-hydrogenases are isolated from Clostridium and Desulfovibrio bacteria, as well as from some green algae, 4. Considerations related to the scale-up of BES such as Chlamydomonas (Jugder et al., 2013). BESs have shown great potential for waste recovery, but large-scale 3.3. Waste to Chemicals with a bioelectrosynthesis cell (BesC) processes have not been developed yet. The need to study and identify the key variables in the scaling up of BES is fundamental; therefore, this Waste to chemical represents the most complex option for chemical section presents a compilation of different BES reported in the literature synthesis through bioelectrochemical conversion. Two large categories from laboratory to industrial implemented BES. stand out in this field: the conversion of CO2 to carbon compounds and The highest TRL (Technology readiness level) value (TRL 9) was the production of bioplastics from wastewater (Bajracharya et al., achieved with MFC, MEC and MES systems, whereas the highest TRL 2017). BESs offer a more sustainable alternative than traditional pro­ reported for the enzymatic system is TRL 3. On the other hand, to the duction methods, avoiding the use of fossil fuels, allowing the recycling best of the author’s knowledge, no pilot-scale studies have been reported of CO2 and valorizing wastewater as raw material. for any of the different enzymatic electrochemical systems. Fig. 5 shows Most studies about MES have been focused on the production of a comparison between the number of total publications and patents methane (Cheng et al., 2009; Su et al., 2016) and acetate, where the reported for each BES technology. It can be inferred that there is a strong latter represents more than 70% of all works reported in the last decade correlation between the highest TRL number achieved by a specific (Jourdin and Burdyny, 2021). Therefore, the involved mechanism is technology and the corresponding number of publications and patents. well-known and the effect of several operational conditions to increase It is worth noting that only a few commercially available products productivity and efficiency has been reported. The productivity of ace­ (TRL 9) have been reported for MFC (L.C.C. Aquacycl, n.d; Microorganic tate reported varies in a wide range between a few to some thousand g/ Technologies Inc, n.d; Plant-e, n.d), MEC (Electro-active Technologies day/m3 depending on the culture type, strain origin, applied potential, Inc., n.d) and MES (Cambrian Innovation Inc, 2021). By searching in the electrode material, and cell configuration, among other main opera­ Scopus database ‘microbial fuel cell’ AND ‘scale-up’, 92 articles were tional parameters (Hengsbach et al., 2022). Recently, the use of mixed found whereas 28 articles were found by searching using ‘microbial cultures has attracted the attention of researchers because it allows to electrolysis cell’ AND ‘scale-up’ as keywords. obtain chemicals with higher economic value than acetate, like middle- Bird et al. (2022) defined some criteria for identifying when an MFC chain fatty acids (Tahir et al., 2021). However, there is no consensus in study can be considered to achieve the pilot-scale level, which can be the scientific community about which strategy, whether mixed or pure extrapolated to the different BES technologies. The criteria consider culture, has more scalability opportunities since both have their pros reactor sizes higher than 10 L, the conduction of the reactor both inside and cons (Chu et al., 2021). Other products obtained by MES are and outside of the laboratory, the operation in either batch or contin­ biodegradable bioplastics, like polyhydroxyalkanoate (PHA) and poly uous mode, operation times longer than one month and the treatment of (3-hydroxybutyrate) (PHB) (Dietrich et al., 2017). Nishio et al. (2013) any waste stream. Using these selection criteria, 30 pilot-scale MFC reported that the production rate of PHB was increased by 60% when an studies in the period between 2008 and 2020 were identified. electrically assisted system was used. The latter was attributed to an There is still little information regarding the TRL 9 BES, like 6 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Fig. 5. Comparison between the number of publications and patents reported for the different BES technologies. Source: Scopus and WIPO, December 2022. EES: enzymatic electrosynthesis; EEC: enzymatic electrolysis cell; EFC: enzymatic fuel cell; MES: microbial electrosynthesis; MEC: microbial electrolysis cell; MFC: mi­ crobial fuel cell. electrode material and reactor configuration, which is attributed to 4.1. Construction of the electrodes safeguarding intellectual property or the competitive edge of the com­ panies. Therefore, to better understand the possibilities regarding the A fundamental component in any electrochemical systems, as well as scale-up of a BES, the studies of TRL 4 and TRL 5 available in the in BESs, is the working electrode. The electrode is responsible for car­ literature will be used. Table 1 shows a summary of the different pilot- rying out the reaction of interest, this being the cause of the various scale BES published in the last 5 years. In this selection, the only studies related to its optimization. Several variables are important for criteria taken into consideration was the size of the reactor (with a the construction and design of the electrodes, this being particularly working volume bigger than 10 L). The working volume is the effective relevant for large-scale applications, where size, surface area and cost volume of the liquid inside the reactor, which considers the anolyte and considerations will determine the feasibility of BES. catholyte (if present). The main characteristics of the cell construction As can be seen in Fig. 6, three are the key variables to be considered like electrode material, reactor volume, separation of the anodic and for the construction of the electrode: chemical composition, shape and cathodic chambers by means of a membrane as well as the type of morphology, and electrode’s modification. microorganism used, waste treated, operational parameters and the The chemical composition is directly related to the base material of performance of the different cells are indicated. It is interesting to note the electrode and its chemical structure, giving the electrode its elec­ that more than 70% of the pilot-scale cells reported in Table 1 consider trochemical characteristic and structural properties but, at the same the use of a membrane for separating the anodic from the cathodic time, directly influencing the type of interaction of the electrode with chamber even if one of the biggest issues related to microbial electro­ the biological catalyst. Shape and morphology are also critical param­ chemical cells is the membrane fouling. Nevertheless, the use of eters in the electrode design, where the required surface area and the ceramic-based membranes, together with carbon-based electrodes desired final application must be taken into consideration. A third highlights the necessity of finding novel cost-effective materials for the consideration is the possible modifications that can be done to the construction of the cells. In addition, ceramic materials have the electrode to improve its properties, such as the increase in the surface advantage of being mechanically and chemically stable, which allows area or in conductivity. Similarly to what occurs with other non- their regeneration by thermal or chemical treatments. COD removal biological emerging electrochemical systems (Ottone et al., 2019), the efficiency and the power density values are typical parameters reported reproducibility of the techniques for electrode construction at a large for comparing the performance of different MFCs. However, an impor­ scale is one of the most important issues in scaling up. tant parameter that is hardly reported among the different pilot-scale As shown in Table 1, carbon-based materials, especially graphite- prototypes is the Net Energy Recovery (NER), which indicates how based, are the most used in scaling-up systems showing a good com­ much energy can be recovered from waste. Only the work published by mercial perspective. Among them, graphite and its derivatives are the Babanova et al. (2020) declares this result. This parameter serves as an most attractive due to their relatively low cost, as shown in Table 2. The indicator of how much energy can be used for other purposes different to advantage of carbon-based materials relies on their lower cost per sur­ waste treatment. NER is a useful parameter of comparison between an face area, since carbon can be easily synthesized in a 3D structure like MFC and other WtP technology. In the case of MECs, there appears to be cloth, felt, and fiber among others. In this table, carbon granules and less consensus on the key parameters to assess performance. For metal wools are not considered for their irregular shape that difficult the instance, COD removal efficiency is not always reported and an impor­ comparison with the same projected area. The data reported in Table 2 tant parameter like the COD to H2 production yield is not calculated. consider only the cost of the material used in the construction of the Other issues related to the scale-up of BESs are the electrode con­ electride. It do not consider the cost of further electrode modifications struction, the addition of a redox mediator, the configuration of the like activation with functional groups nor thermal and chemical treat­ reactor and the downstream steps. These points will be discussed in ments of the base material. detail below. 7 D. Maureira et al. Table 1 Specifications of pilot-scale BES published between 2018 and 2022. BES Waste Working Membrane Anode material Cathode Biological agent Performance Stable Operational REF Volume (projected area) material phase Parameters (L) (projected operation area) time (d) ceramic graphite felt air COD removal: 93.52%, I: domestic membrane graphite felt cathode (0.706 anaerobic microbial 43.7 mA, Pd: 23.52 fed-batch mode, HRT: (Suransh MFC wastewater 36 (vermiculite) (0.756 m2) m2) consortium mW⋅m− 3, Ceff: 3% 92 2–3 d et al., 2023) graphite rod graphite rod (0.003 m2) with (0.003 m2) with granular activated sludge from the dairy granular graphite graphite bed (n. industrial plant treating the COD removal: 82%, Pd: semi-continuous flow (Callegari MFC wastewater 0.855 CEM bed (n.a.) a.) dairy waste samples 26.5 W⋅m− 3, Ceff: 24%, 65 mode, f: 1 L⋅d− 1 et al., 2018) continuous flow domestic carbon fiber brush carbon air effluent of previous mode, HRT: 12 h, f: (Rossi et al., MFC wastewater 850 no membrane (11 m2) cathode (20 m2) bioelectrochemical systems COD removal: 49% 100 5.76 L⋅min− 1⋅m− 2 2022) Fimbristylis ferruginea with bacterial community from rhizospheric soils of plants COD removal: 74.1%, 316 stainless growing at textile ADMI removal: 97.32%, textile dye 316 stainless steel steel sheets wastewater Pd: 197.94 mW⋅m− 2 (at (Patel et al., MFC wastewater 30 CEM sheets (0.0126 m2) (0.0126 m2) polluted site 500 Ω) 4 batch mode, HRT: 2d 2021) COD removal: 81.67%, batch mode, cycle (Selvaraj and domestic graphite plate graphite plate Pd: 24.104 mW⋅m− 2, i: volume: 20 L, total Velvizhi, MFC wastewater 43.88 no membrane (0.848 m2) (0.848 m2) macrophyte plants 23.844 mA⋅m− 2 45 cycles: 3 2023) COD removal: 65%, Ceff: 27%, i: 103 mA⋅m− 2 (at gas diffusion 47 Ω), Pd: 92 mW⋅m− 2, continuous flow 8 − 1 swine graphite fiber cathodes (0.07 NER: 0.11 kWhr⋅kgCOD (at mode, HRT: 4 h, f: (Babanova MFC wastewater 110 no membrane brushes (1.2 m2) m2) lagoon sediment 330 Ω) 170 660 L⋅d− 1 et al., 2020) graphite felt coated with CuSn on air plant secondary continuous flow (Nath and synthetic ceramic graphite felt facing side metabolites treated Pd. 4.0 mW⋅m− 2, Ceff: 5% mode, f: 150 Ghangrekar, MFC wastewater 125 membrane (0.027 m2) (0.027 m2) anaerobic sludge (at 1 Ω), I: 40 mA (at 1 Ω) 160 mL⋅min− 1 2020) graphite rod Pd: 10.3 W⋅m− 3, I: 285 synthetic (0.022 m2) with secondary wastewater mA (at 150 Ω), Ceff: continuous flow textile granular activated graphite rod sludge from the distillery 10.67% (at 150 Ω), mode, f: 0.72–1.2 (Nakhate UASB-MFC wastewater 12.09 no membrane carbon bed (n.a.) (0.011 m2) industry COD removal: 71.73% 46 L⋅h− 1, HRT: 13.88 h et al., 2019) digestate from a local fed-batch mode, cycle pig slurry graphite felt (0.18 graphite felt Wastewater Treatment H2 production rate: 0.2 duration 2–5 d, f: 15 (San-Martín MEC liquid fraction 16 CEM m2 ) (0.18 m2) Plant LH2⋅L− 1⋅d− 1 5 L⋅h− 1, E: 1 V et al., 2019) 316 stainless ultra-high steel flat mesh continuous flow molecular with stainless mode, HRT: 5 h, f: Biotechnology Advances 64 (2023) 108123 domestic weight graphite felt (1.44 steel wire wool microorganism from the 150 mL⋅min− 1, E: 0.9 (Verbeeck MEC wastewater 45 polyethylene m2 ) (0.6 m2) same wastewater H2 purity: 92.8% 100 V et al., 2018) graphite felt (1.2 ultra-high m2) encased by molecular two sheets of 438 grade 1 continuous flow domestic weight stainless steel stainless steel microorganism from the mode, HRT: 24 h, f: (Verbeeck MEC wastewater 135 polyethylene mesh wool (n.a.) same wastewater H2 purity: 98.4% 100 75 mL⋅min− 1, E: 1.2 V et al., 2018) granular continuous flow synthetic granular graphite graphite bed (n. activated sludge (anode), COD removal: 56%, I: 86 mode, f: 6 L⋅d− 1, HRT: (Zeppilli et al., MEC wastewater 12 AEM bed (n.a.) a.) anaerobic sludge (cathode) mA, Ceff: 13% 140 12.6 h, anode 2020) (continued on next page) D. Maureira et al. Table 1 (continued ) BES Waste Working Membrane Anode material Cathode Biological agent Performance Stable Operational REF Volume (projected area) material phase Parameters (L) (projected operation area) time (d) potential: 0.2 V vs. SHE − 2 i: 0.27 A⋅m , Ceff: 10%, activated sludge (anode), TOC removal: 80%, TN wastewater collected from removal: 70%, specific MEC with domestic graphite felt (2.35 graphite felt the denitrification zone energy consumption of continuous flow (Maria et al., denitrification wastewater 150 AEM m2) (2.35 m2) (cathode) 0.18 kWh⋅m⋅L− 3 63 mode, HRT: 1d, E: 1 V 2018) 316 L stainless COD removal rate (AC): steel frames with electrode pieces from 0.83 g⋅d− 1⋅L− 1, acetate continuous flow mode carbon tissue 316 L stainless previous production rate (CC): (AC), f: 45 mL⋅d− 1, E: biowaste strips fixed steel baskets bioelectrochemical systems 0.53 g⋅d− 1 ⋅L− 1, acetate 0.6–1.2 V, CO2 flow hydrolyzate between two filled with (anode). Fermentation licor maximum concentration: rate (CC): ~ 1.5 (AC), CO2 AEM and CEM stainless steel carbon granules of different food wastes 8.3 g⋅L− 1, i: 2 A⋅m− 2, Ceff: mL⋅s− 1, recirculation (Tian et al., MES (CC) 12.5 frame grills (0.36 m2) (0.36 m2) (cathode) 98.6% 55 flow (CC): 100 L⋅h− 1 2023) batch mode (liquid) 9 with continuous gas Methane production rate: flowing, HRT of gas: (Enzmann and graphite cloth graphite cloth 11.7 mmol⋅d− 1, i: 85 33 min, E: − 1100 mV Holtmann, MES CO2 50 CEM (0.75 m2) (1.59 m2) Methanococcus maripaludis mA⋅m− 2, Ceff: 100% 3.33 vs. Ag/AgCl 2019) Nomenclature: AC: anodic chamber, ADMI removal: American Dye Manufacturer’s Institute removal efficiency, AEM: anion exchange membrane, BES: bioelectrochemical system, CC: cathodic chamber, Ceff: maximum coulombic efficiency, CEM: cation exchange membrane, COD removal: chemical oxygen demand removal efficiency, E: potential difference, f: flow rate, HRT: hydraulic retention time, I: highest current, i: highest current density, MEC: microbial electrolysis cell, MFC: microbial fuel cell, MES: microbial electrosynthesis, n.a.: not applicable, NER: net energy recovery, Pd: Highest power density, SHE: standard hydrogen electrode, UASB: upflow anaerobic sludge blanket. Biotechnology Advances 64 (2023) 108123 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Fig. 6. Schematic representation of the key variables in electrode manufacturing. Table 2 Comparison of the cost of different electrode configurations used in BESs considering 1 m2 of projected area. Electrode Material Specification Cost (Dólar) for 1 m2 projected Total surface area Specific cost (USD/total Source Dimensions area (m2) area) 3D Cloth 1900 478 4,0 Fuel cell store 3D Felt 856 66,3 12,9 Fuel cell store 2D Graphite Paper 469 1 468,8 Fuel cell store Sigma 2D Plate 2110 1 2110,0 Aldrich Sigma 3D Nanotubesa 9700 80,000 0,1 Aldrich Graphene Sigma 2D Paper 671 1 671,0 Aldrich Sigma 3D Glassy carbon Plate 3519 N.D. N.D. Aldrich Platinum Sigma b 2D 99.95% Thin layer 2854 1 2853,5 Aldrich Sigma 2D Stainless steel Sheet 1001 1 1000,8 Aldrich a 2 Considering a loading of 100 g of nanotubes per m . b For a 100 nm deposited thin layer. The cost of the support material is not considered. 4.1.1. Chemical composition and semiconductors (ZnO and TiO2), have emerged with attractive The chemical composition is directly related to the materials used in electrochemical and mechanical properties (Ottone et al., 2014a, 2014b; the fabrication of the electrodes; here carbon and metal-based groups Ottone et al., 2021b). However, these new materials are still under stand out. Among the family of carbon-based materials, graphite, gra­ development for industrial use (Jaouen and Morozan, 2014; Liao et al., phene, and glassy carbon electrodes can be found. Carbon-based mate­ 2018; Vikrant et al., 2017), so they are not considered in this review. rials have some properties that make them attractive for electrochemical Carbon and metal-based materials are the most used in the fabrica­ applications, such as good electrical conductivity and low resistance, tion of electrodes, and the literature highlights some of their advantages high biocompatibility and chemical stability, resistance to corrosion, such as the cost of production, high specific surface area and biocom­ large surface area, appropriate mechanical strength and toughness patibility (Liu et al., 2020b; Ahn and Logan, 2010; Huong Le et al., 2017; (Dubey and Guruviah, 2019; Thamilselvan et al., 2016). Lin et al., 2019; Liu et al., 2004; Mohanakrishna et al., 2018; Rengaraj Metal-based electrodes have been widely studied also, and certain et al., 2011; Zhou et al., 2011). metals with good characteristics (conductivity, corrosion resistance, and Carbon-based electrodes are also attractive from a cost perspective, chemical reactivity) for use in electrochemical cells are recognized. being significantly cheaper than metals widely used in electrochemistry, Some of the most used metals for electrochemical applications are such as platinum and copper. This makes carbon-based electrodes copper, platinum, titanium and stainless steel (Terzi et al., 2019). extremely attractive for the construction of large-scale BES. Graphite- Among them, stainless steel is an excellent material alternative for based electrodes are particularly suitable when considering the design electrode manufacturing at large scale, with outstanding properties such of large-scale BES. Graphite-based electrodes do not need to be sup­ as corrosion resistance, high electric conductivity and low cost ported, can be easily subjected to bulk or surface modifications in order compared to other metals. To increase the surface area, stainless steel to improve their electrochemical and physical qualities, and are readily foams have been proposed, showing robustness and biocompatibility to available from different commercial suppliers. form biofilms for MFC applications (Kalathil et al., 2018). Recently, new materials, such as metal organic frameworks (MOFs) 10 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 4.1.2. Shape and morphology topography influences the bacterial adhesion to the surface or the bio­ The shape and morphology of the electrode plays an important role film formation, and it has been reported that bacteria preferably colo­ in its construction. Based on the forms, they can be categorized as: sheets nize porous, grooved and braided surfaces (Yuan et al., 2018; Flint et al., or plates, foams, nanotubes and fibers, materials based on cross linking 2000; Whitehead and Verran, 2006). In reactions catalyzed by enzymes, or woven units. Different presentations have been developed to increase the surface area of the electrode also plays an important role. The the specific surface area of the electrode, which is key to achieve better available surface area will determine the number of functional groups current densities and serve as catalyst support (Artsanti et al., 2017; that can be added and, therefore, the enzyme load immobilized on the Debe, 2011; Gude, 2016). electrode (Camelin et al., 2022). An interesting review of some cases of Sheets or plates are the usual and basic shape of electrodes, despite different techniques for protein and enzyme coupling on electrodes has the low amounts of catalysts that can be loaded. This limitation is due to been recently published (Olloqui-Sariego et al., 2021). the low exposed area, as in MFC (Fu et al., 2012; Li et al., 2009; Zhao As already mentioned, the most attractive materials for the con­ et al., 2009). The power densities observed for a MFC using a plate struction of a bioelectrode are carbon and metal-based, but in terms of electrode were the lowest when compared to other electrode shapes, their ability to be modified, carbon-based electrodes have an advantage. such as mesh or cylinder (Fu et al., 2012). The foam electrode structure This makes them extremely attractive to be used in the construction of presents a higher surface area compared with plane plate or sheet, electrodes for large-scale operation. resulting in an improvement on the electrochemical performance (Ali et al., 2014; Liu and Liang, 2000; Montillet et al., 1994; Sen et al., 2014). 4.2. Addition of redox mediators Among the different materials to be used, carbon-based foams have been recognized as exceptional due to their excellent properties, like high The selection of the BES arrangement will depend on the system to be electrical conductivity (Degirmenci and Kirca, 2018; Wang et al., 2015). mounted and the mediator to be used. The use of a free form of RM is Another of the most widely used forms reported in the literature are recommended in cases where the mediator is cheap and environmen­ nanotubes and fibers, which can be used to build up more complex tally benign. On the contrary, in those cases where the subsequent waste structures. Nanotubes and fibers are categorized in the same group treatment is not efficient enough to eliminate the RM, their commercial despite their difference in size, which are about 0.4 nm and in the range value is high, or poorly soluble in the medium, immobilization will be of 5 to 10 μm of diameter, respectively (Bhatt and Goe, 2017; Peng et al., required to achieve good results (Azhar et al., 2005; Motabar et al., 2000). Nanotubes and fibers have been also carbon-based electrodes 2021). Kochius et al. (2012) described in detail the immobilization whose characteristics, like high mechanical strength and ductility, have techniques available for redox mediators. been highlighted for electrode manufacturing. Moreover, excellent sta­ RM can be used with different purposes depending on what is being bility and conductivity have been attributed to carbon nanotubes (Zhou targeted: increasing in pollutant removal efficiency or increasing in et al., 2011). production efficiency. As an example, Sevda and Sreekrishnan (2012) Lastly, materials formed from interlocking or woven units ca be observed that using RMs on MFC for the treatment of sewage and found which are constructed in paper-like, cloth-like and felt-like simultaneous generation of energy, a significant improvement on the shapes. Their structure is based on fibers or nanotubes, either inter­ removal of organic matter was obtained with the use of methylene blue woven (for cloth) or non-structured (for felt) (Huong Le et al., 2017; Kim or neutral red, but this good performance was not reflected in terms of et al., 2019), while in paper the fibers are held together in a resin matrix energy production. Authors attributed this behavior to an alteration on (Radhakrishnan and Haridoss, 2011). Developing a structure based on the cellular metabolism caused by the RM at the level of perturbation in woven/ interlaced fibers or nanotubes has been found to improve the the NADH/NAD+ ratio leading to an imbalance in cofactors which mechanical properties, in this way being possible to provide strength, participate in many metabolic reactions (Ieropoulos et al., 2005). stiffness and toughness to the electrodes (Dan-Mallam et al., 2015). Tamirat et al. (2020) highlighted some characteristics of RMs that should be met for its selection, such as high reversibility, fast kinetics, 4.1.3. Electrode modifications high solubility, and negligible side reactions. Table 3 presents a list of All the materials, shapes and structures described before can be the most studied RMs that are compatible with microbial or enzymatic modified to improve its electrochemical performance. These modifica­ systems. tions have been classified as follows: hybrid porous, hybrid surface The studies regarding RM are focusing mostly on the kinetics of nanostructures and decoration of electrodes surfaces. The first class, different redox mediators in conjunction with different substrates and hybrid porous, is based on those primary porous structures which are the analysis of their response at the level of pollutant removal, power filled with another material with a high surface area; an example of this generation and/or production of products of interest. An example of the is the reticulated vitreous carbon foam, whose micro holes can be filled enhancing effect of some RM on BES is the effect of different concen­ with nanofibers (Walsh et al., 2016). The second class, hybrid surface trations of methylene blue (MB) over MFC systems where reported re­ nanostructure, although defined as “tubes within tubes” is described as sults show that the highest values of energy and electric current an arrangement of surface geometry with micropores filled with generated were observed with 0.3 mM (Rahimnejad et al., 2011) and microtubes; an example of this technique is the use of nanotubular ti­ 0.08 mM (Sevda and Sreekrishnan, 2012). These results highlight the tanates which were incorporated inside the pores of a wide nanotube peculiarity of each system and the need to optimize the addition of RM, array by electrophoretic deposition (Bavykin et al., 2013). The last in order to obtain the best possible results. category is based on the deposition or decoration of nanoparticles on the RM plays an important role in BES, and it can be applied in two electrode surface; this can be carried out by combining different tech­ formats: free form or immobilized on a support. Different studies have niques, such as redox gel for coating, electrochemical deposition and shown the use of free RM on BES, but this has a clear disadvantage reduction of metal salts, among others. In the literature, this kind of because its recovery from the reaction solution is difficult or impossible modification is mainly focused on the deposition of metal on carbon- with the corresponding environmental threat (Dai et al., 2016). based materials (Dhibar and Das, 2014; Fattahi et al., 2011; Han Although the concentrations of RM used are in the order of μM or mM, et al., 2018; Jeromiyas et al., 2019; Quinn et al., 2005; Vaghari et al., the need for their continuous feeding makes them a heavy economic and 2016; Wang et al., 2007; Xia et al., 2015). More information regarding environmental burden. To solve this, many studies use RMs in an these modification techniques can be found in Walsh et al. (2016). immobilized form, thus, retention and reuse are favored. The use of RM Carbon-based materials have the best relationship between physical has been shown to have a positive effect on BES, but the use in stoi­ properties, such as specific surface area, and electrochemical properties. chiometric quantities is not feasible for the operation of continuous The surface area available is extremely important because the material systems due to its high commercial price (Hollmann et al., 2006). It has 11 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Table 3 Redox mediators and some of their characteristics. Redox mediator Redox potential (vs Solubility in Cost (USD/ Form Reference SHE) water* g)** Free/ Methylene blue (MB) − 0.1 43.6 g/L 3.12 Thiele et al., 2008 immobilized Methyl viologen (MV) − 0.446, − 0.760 620 g/L 49.8 Free Aulenta et al., 2007 Neutral red (NR) − 0.325 50 g/L 41.7 Free Harrington et al., 2015 Riboflavin (RI) – Poor 17.3 Free Field and Brady, 2003 Poor Cobaltocene (CO) − 1.88, − 0.94 (vs SCE) 54.2 Immobilized Zhao et al., 2015 (<1 g/L) Phenazine methosulfate (PMS) +0.08 200 g/L 47.1 Free Thiele et al., 2008 Anthraquinone-1,6-disulfonic acid (AQDS) − 0.184 – – Immobilized Aulenta et al., 2010 Benzoquinone (BE) +0.28 Poor 4.1 Immobilized Hendler, 1977 Poor Naphthoquinone (NA) − 0.145 6.7 Immobilized Meckstroth et al., 1981 (3.5 g/L) 2,2 -azino-bis(3-ethylbenzo- thazoline-6-sulphonc acid) ′ Free/ 0.670 50 g/L 69 Tsujimura et al., 2001 (ABTS) immobilized * Solubility defined at 25 ◦ C and obtained from PubChem data base. ** Data obtained from SigmaAldrich catalogue. been shown that the systems of RM removal are inefficient and it is known that, even at low concentrations, they can be environmentally hazardous (Azhar et al., 2005; Novotný et al., 2011). Therefore, the alternative of immobilizing RMs has become quite attractive and different immobilization strategies have been reported, such as adsorption, polymerization, entrapment and covalent linkage. More information at this respect can be found in Kochius et al. (2012). 4.3. Reactor configuration The configuration of the electrochemical cell or reactor is also a key issue for the implementation of BES in a commercial application. Different configurations have been proposed, using one, two or three chambers. The main advantage of using one chamber relies on its simplicity; however, as all products are in a unique chamber, the downstream process become more complex. Therefore, the use of two chambers in which the anolyte and catholyte products are separated has been considered a preferable alternative. This two-chamber configura­ tion allows for higher efficiencies since an ion exchange membrane is used to generate the two compartments, thus avoiding reverse reactions, minimizing side reactions and obtaining cathodic products of higher purity (Tiquia-Arashiro, 2020). However, one of the disadvantages of this configuration when using wastewater as a substrate is the mem­ brane fouling (Hiegemann et al., 2019), i.e., due the accumulation of Fig. 7. Schematic representation of a plate and frame reactor. Blue and red some of the particulate materials present in the waste stream (Hou et al., electrodes represent the anode and cathode respectively. (For interpretation of 2021). the references to colour in this figure legend, the reader is referred to the web The most prominent advances in reactor configuration have been in version of this article.) MFC systems, in which the plate-and-frame reactor proved to be a very convenient and versatile configuration. The plate and frame reactor, as 2010). Some of these criteria are geometric similarity, such as hydraulic shown in Fig. 7, presents a sandwich-style configuration, where the ion retention time (HRT), specific power input (SPI), Reynolds rotation exchange plate and the electrodes are trapped between a series of plates number (Re) and stirrer tip speed (STS). However, in the scale-up of and frames. With this type of configuration, scaling up the process is bioelectrochemical reactors there is no consensus in the research com­ quite easy, by simply adding more modules to increase the cell volume munity about which criteria should be taken into consideration. (González-García et al., 2000). The main downside of this configuration Considering that a large-scale BES will work in continuous mode and is the poor or almost non-existent mixing and homogenization; to solve the relevance of maintaining the energy requirements, HRT and SPI this, different alternatives have been studied, such as the management of have been considered for some scale-up BES reactors (Dekker et al., the inlet flow and the use of flow dispensers in the middle of the reaction 2009; Fitschen et al., 2019; Haavisto et al., 2017; Walter et al., 2016; Ye chambers (Arenas et al., 2020). In addition, an improved design is the et al., 2020). Other parameters proposed in the literature are specific inclusion of air cathodes which report positive effects comparing current density, electrode spacing and electrode geometry (Cotterill different MFC reactor configurations (Rossi and Logan, 2022). In air et al., 2017; Jadhav et al., 2021; Janicek et al., 2014; Papillon et al., cathodes MFC, the oxygen in air can passively flows to the cathode 2021). On the other hand, Reynolds rotation number or stirrer tip speed through a hydrophobic layer without need of pumps and thus energy have been less proposed, since few MFC and MEC reactors have no consumption. agitation (Pan et al., 2019). In microbial fermentation processes, there are some criteria that permit the design of large-scale processes leading to the same produc­ tivity and product quality as that developed at a laboratory scale (Yang, 12 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 5. Challenges and future perspectives for BES technologies life cycle assessment (LCA) methodology of different BESs is reported elsewhere (Savla et al., 2021). Thus, MFC and MEC are still far from Among the different BES technologies, MFC and MEC are the most being able to compete with ongoing technologies in high throughput developed systems with the greatest potential for commercial imple­ wastewater treatment plants. However, a feasible option for this tech­ mentation in the near future. In particular, MFC technology is gaining nology is wastewater treatment in small rural communities, where significance for wastewater treatment because of its advantages with throughputs and workloads are much lower (Nagendranatha Reddy respect to the conventional technology of activated sludge which con­ et al., 2018). Nevertheless, from an economic point of view, the reve­ sumes much energy due to the requirement of constant aeration. How­ nues related to the treatment of the waste are a key factor to consider in ever, certain aspects still require of improvements, such as reducing the the equation that could lead to a positive net present value (NPV) in a cost of currently expensive electrode materials, proper wastewater pH techno-economic analysis. control, and biofilm growth on the electrode’s surface (Waller and Moreover, it has been demonstrated that it is possible to use a MEC Trabold, 2013). The intensification of the BES processes is a key strategy for the treatment of waste activated sludge (WAS) (Hu et al., 2019), for achieving the commercialization level of the technology, analogous which arises as a promising application of BESs because the accumula­ to what has been proposed for other biochemical processes (Boodhoo tion of WAS is a big problem in traditional wastewater treatment plants et al., 2022). (Lu et al., 2012). In addition, among the different biological strategies to The differences between laboratory conditions and relevant envi­ produce hydrogen, MEC has been defined as the most promising tech­ ronmental conditions need to be taken into consideration for reaching nology due to its better control over hydrogen generation rate and the market. The variation of substrate parameters, including tempera­ effective conversion of organic feedstock, regardless of thermodynamic ture, pH, concentrations and components, is an important issue to have limits (Qyyum et al., 2022). The latter suggests that MEC technology will into consideration (Sulaymon and Abbar, 2012). Therefore, good design achieve a rapid advance toward maturity. of pilot-scale experiences is necessary for giving useful information for offering attractive BES-based solutions. Interestingly, wastewater 6. Conclusions treatment in small rural communities, where throughputs and work­ loads are much lower, rises as a feasible option for introducing BES BES systems have been studied from different perspectives, such as technology (Nagendranatha Reddy et al., 2018). biocatalyst components, electrochemical reactor configuration and Another important parameter to consider in BES technology is COD electrode construction, among others. However, much more applied removal efficiency. It was reported that the limit of COD removal with research is needed for its commercial application. Such efforts should be MFC is 1.1 kg COD/(m3d), which represents between 60 and 70% of primarily focused on electrode manufacture optimization since it is one COD removal from the original affluent (de Fouchécour et al., 2022). On of the main factors affecting investment costs. For this reason, areas such the other hand, traditional wastewater treatment (aerobic and anaer­ as material for electrode construction and techniques of electrode obic) leads to COD removal yields over 90% and, most importantly, it is modification to ensure a better biocatalyst attachment to the electrodes possible to reach a final COD concentration below the disposal standards are critical to be further developed. Although different materials have (Aziz et al., 2019), something that it is not possible to reach with current been studied for electrode fabrication, the high production costs asso­ BES technologies. Each region has its own discharge standards; how­ ciated to the difficult scale-up of the synthesis procedures for electrode ever, the limit of COD concentrations varies between 125 mg/L to 60 manufacture is a crucial issue that needs to be addressed to become a mg/L (Deng and Wheatley, 2016; EPA, 2001; E. U. W. Directive, 1991). competitive technology. Since BESs lead to lower COD removal yields than traditional waste­ Among the different BES, the microbial cells stand out as the most water treatment, it should be highlighted that the purpose of their promising technology to expand their applications to reach technolog­ implementation is to have a higher energy recovery and allow their ical significance in the short term because of their advances in tech­ coupling to another traditional treatment system to reach a COD value nology implementation and R&D investment compared to the enzymatic below the disposal regulation parameters. Related to COD removal, technologies mentioned. It is necessary that the BES technologies that other reactor design parameters arise, like organic loading rate (OLR) are in lower TRL values, such as enzymatic electrochemical cells, learn and volumetric treatment rate (VTR), from which hydraulic retention from the knowledge reached with the already commercially available time (HRT) can be obtained (Baeza et al., 2017). Thus, the requirements technologies to accelerate their development and thus reach the for waste treatment are a key factor in introducing BES technology as a competitive level in a short period of time. competitive solution. BES seems to be disadvantageous when compared to conventional Funding technologies. For instance, the highest hydrogen production rate re­ ported with a pilot-scale MEC using urban wastewater is 0.004 Nm3/ This work was supported by FONDECYT [grant number 11180967]; d (Baeza et al., 2017), which is considerably lower than obtained with a Beca Doctorado Nacional [grant number 21190467 - Agencia Nacional polymer exchange membrane (PEM) electrolyzer that arrives at 720 de Investigación y Desarrollo (ANID), Chile]. Nm3/h (Dincer and Acar, 2015). In the case of MFC, the highest power density reported with a pilot-scale reactor is 60 W using a 1000 L reactor Declaration of Competing Interest for treating municipal wastewater, which is still orders of magnitude lower than that produced with a proton exchange membrane fuel cell None. (PEMFC), which varies from 1 to 100 kW (Felseghi et al., 2019). Thus, with current materials used in the construction of the cells, the cost of Data availability using BES for wastewater treatment is still significantly higher than activated sludge or anaerobic digestion (Rozendal et al., 2008). Ac­ Data will be made available on request. cording to a study performed by Christodoulou et al. (2017), formic acid is the product that can be produced by means of a MES with the lowest References production cost (0.49 £/kg), which is a competitive cost with respect to traditional production systems. However, the current investment costs Ahn, Y., Logan, B.E., 2010. Effectiveness of domestic wastewater treatment using associated with MES are higher than that of conventional technologies, microbial fuel cells at ambient and mesophilic temperatures. Bioresour. Technol. 101 (2), 469–475. https://doi.org/10.1016/j.biortech.2009.07.039. which represents the most important limitation for investors. A com­ Ali, I., Khan, T., Omanovic, S., 2014. Direct electrochemical regeneration of the cofactor plete study of techno-economic analysis and sustainability through the NADH on bare Ti, Ni, Co and Cd electrodes: the influence of electrode potential and 13 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 electrode material. J. Mol. Catal. A Chem. 387, 86–91. https://doi.org/10.1016/j. Camelin, E., Romero, O., Piumetti, M., Ottone, C., Illanes, A., Fino, D., 2022. Mechanisms molcata.2014.02.029. of interaction among enzymes and supports. In: Nanomaterials for Biocatalysis. Al-Sahari, M., Al-Gheethi, A., Mohamed, R.M.S.R., Noman, E., Naushad, M., Rizuan, M. Elsevier, pp. 105–148. https://doi.org/10.1016/B978-0-12-824436-4.00022-8. B., Vo, D., Ismail, N., 2021. Green approach and strategies for wastewater treatment Chandrasekhar, K., Kumar, A.N., Raj, T., Kumar, G., Kim, S.H., 2021. Bioelectrochemical using bioelectrochemical systems: a critical review of fundamental concepts, system-mediated waste valorization. Syst. Microbiol. Biomanuf. 1 (4), 432–443. applications, mechanism, and future trends. Chemosphere 285, 131373. https://doi. https://doi.org/10.1007/s43393-021-00039-7. org/10.1016/j.chemosphere.2021.131373. Chenevier, P., Mugherli, L., Darbe, S., Darchy, L., DiManno, S., Tran, P.D., Valentino, F., Alsayed, A., Soliman, M., Eldyasti, A., 2020. Microbial fuel cells for municipal Iannello, M., Volbeda, A., Cavazza, C., Artero, V., 2013. Hydrogenase enzymes: wastewater treatment: From technology fundamentals to full-scale development. application in biofuel cells and inspiration for the design of noble-metal free Renew. Sust. Energ. Rev. 134 (February), 110367 https://doi.org/10.1016/j. catalysts for H2 oxidation. Comptes Rendus Chimie 16 (5), 491–505. https://doi. rser.2020.110367. org/10.1016/j.crci.2012.11.006. Álvarez, A., Bansode, A., Urakawa, A., Bavykina, A.V., Wezendonk, T.A., Makkee, M., Cheng, S., Xing, D., Call, D.F., Logan, B.E., 2009. Direct biological conversion of Gascon, J., Kapteijn, F., 2017. Challenges in the greener production of formates/ electrical current into methane by electromethanogenesis. Environ. Sci. Technol. 43 formic acid, methanol, and DME by heterogeneously catalyzed CO2 hydrogenation (10), 3953–3958. https://doi.org/10.1021/es803531g. processes. Chem. Rev. 117 (14), 9804–9838. https://doi.org/10.1021/acs. Chorbadzhiyska, E., Hubenova, Y., Hristov, G., 2011. Microbial electrolysis cells as chemrev.6b00816. innovative technology for hydrogen production. Workshop “Renewable Energy Arenas, L.F., Ponce de León, C., Walsh, F.C., 2020. The versatile plane parallel electrode Technologies”, pp. 422–427. geometry: An illustrated review. J. Electrochem. Soc. 167 (2), 023504 https://doi. Christodoulou, X., Okoroafor, T., Parry, S., Velasquez-Orta, S.B., 2017. The use of carbon org/10.1149/1945-7111/ab64ba. dioxide in microbial electrosynthesis: advancements, sustainability and economic Artsanti, P., Sudarlin, S., Kirana, E.F., 2017, October. The effect of increasing surface feasibility. J. CO2 Utiliz. 18, 390–399. area of graphite electrode on the performance of dual chamber microbial fuel cells. Chu, N., Hao, W., Wu, Q., Liang, Q., Jiang, Y., Liang, P., Zeng, R.J., 2021. Microbial In: Proceeding International Conference on Science and Engineering, Vol. 1, electrosynthesis for producing medium chain fatty acids. Engineering 16, 141–153. pp. 137–140. https://doi.org/10.14421/icse.v1.284. Chung, Y., Tannia, D.C., Kwon, Y., 2018. Glucose biofuel cells using bi-enzyme catalysts Aulenta, F., Catervi, A., Majone, M., Panero, S., Reale, P., Rossetti, S., 2007. Electron including glucose oxidase, horseradish peroxidase and terephthalaldehyde transfer from a solid-state electrode assisted by methyl viologen sustains efficient crosslinker. Chem. Eng. J. 334, 1085–1092. https://doi.org/10.1016/j. microbial reductive dechlorination of TCE. Environ. Sci. Technol. 41 (7), cej.2017.10.121. 2554–2559. https://doi.org/10.1021/es0624321. Cocuzza, C., Pietricola, G., Zonca, I., Dosa, M., Romero, O., Tommasi, T., Piumetti, M., Aulenta, F., di Maio, V., Ferri, T., Majone, M., 2010. The humic acid analogue 2022. Simultaneous CO2 reduction and NADH regeneration using formate and antraquinone-2,6-disulfonate (AQDS) serves as an electron shuttle in the electricity- glycerol dehydrogenase enzymes co-immobilized on modified natural zeolite. RSC driven microbial dechlorination of trichloroethene to cis-dichloroethene. Bioresour. Adv. 12 (48), 31142–31155. Technol. 101 (24), 9728–9733. https://doi.org/10.1016/j.biortech.2010.07.090. Cormos, A.-M., Szima, S., Fogarasi, S., Cormos, C.-C., 2018. Economic assessments of Azhar, S.S., Liew, A.G., Suhardy, D., Hafiz, K.F., Hatim, M.D.I., 2005. Dye removal from hydrogen production processes based on natural gas reforming with carbon capture. aqueous solution by using adsorption on treated sugarcane bagasse. Am. J. Appl. Sci. Chem. Eng. Trans. 70, 1231–1236. https://doi.org/10.3303/CET1870206. 2 (11), 1499–1503. https://doi.org/10.3844/ajassp.2005.1499.1503. Cotterill, S.E., Dolfing, J., Jones, C., Curtis, T.P., Heidrich, E.S., 2017. Low temperature Aziz, A., Basheer, F., Sengar, A., Khan, S.U., Farooqi, I.H., 2019. Biological wastewater domestic wastewater treatment in a microbial electrolysis cell with 1 m2 anodes: treatment (anaerobic-aerobic) technologies for safe discharge of treated towards system scale-up. Fuel Cells 17 (5), 584–592. slaughterhouse and meat processing wastewater. Sci. Total Environ. 686, 681–708. Creasey, R.C.G., Mostert, A.B., Nguyen, T.A.H., Virdis, B., Freguia, S., Laycock, B., 2018. Babanova, S., Jones, J., Phadke, S., Lu, M., Angulo, C., Garcia, J., Carpenter, K., Microbial nanowires – electron transport and the role of synthetic analogues. Acta Cortese, R., Chen, S., Phan, T., Bretschger, O., 2020. Continuous flow, large-scale, Biomater. 69, 1–30. https://doi.org/10.1016/j.actbio.2018.01.007. microbial fuel cell system for the sustained treatment of swine waste. Water Environ. Cristina, G., Camelin, E., Ottone, C., Garofalo, S.F., Jorquera, L., Castro, M., Fino, D., Res. 92 (1), 60–72. https://doi.org/10.1002/wer.1183. Schiappacasse, M., Tommasi, T., 2020. Recovery of humic acids from anaerobic Baeza, J.A., Martínez-Miró, Á., Guerrero, J., Ruiz, Y., Guisasola, A., 2017. sewage sludge: Extraction, characterization and encapsulation in alginate beads. Int. Bioelectrochemical hydrogen production from urban wastewater on a pilot scale. J. Biol. Macromol. 164, 277–285. https://doi.org/10.1016/j.ijbiomac.2020.07.097. J. Power Sources 356, 500–509. Dai, R., Chen, X., Ma, C., Xiang, X., Li, G., 2016. Insoluble/immobilized redox mediators Bahar, T., Yazici, M.S., 2018. Immobilized glucose oxidase biofuel cell anode by for catalyzing anaerobic bio-reduction of contaminants. Rev. Environ. Sci. MWCNTs, ferrocene, and polyethylenimine: Electrochemical performance. Asia Pac. Biotechnol. 15 (3), 379–409. https://doi.org/10.1007/s11157-016-9404-z. J. Chem. Eng. 13 (1), e2149 https://doi.org/10.1002/apj.2149. Dan-Mallam, Y., Hong, T.W., Abdul Majid, M.S., 2015. Mechanical characterization and Bajracharya, S., Srikanth, S., Mohanakrishna, G., Zacharia, R., Strik, D.P., Pant, D., 2017. water absorption behaviour of interwoven kenaf/PET fibre reinforced epoxy hybrid Biotransformation of carbon dioxide in bioelectrochemical systems: state of the art composite. Int. J. Polym. Sci. 2015 https://doi.org/10.1155/2015/371958. and future prospects. J. Power Sources 356, 256–273. https://doi.org/10.1016/j. de Fouchécour, F., Larzillière, V., Bouchez, T., Moscoviz, R., 2022. Systematic and jpowsour.2017.04.024. quantitative analysis of two decades of anodic wastewater treatment in Bandyopadhyay, A., Stöckel, J., Min, H., Sherman, L.A., Pakrasi, H.B., 2010. High rates bioelectrochemical reactors. Water Res. 118142 https://doi.org/10.1016/j. of photobiological H2 production by a Cyanobacterium under aerobic conditions. Nat. watres.2022.118142. Commun. 1 (1), 1–7. https://doi.org/10.1038/ncomms1139. Debe, M.K., 2011. Effect of electrode surface area distribution on high current density Barlett, P., 2008. In: Barlett, P. (Ed.), Bioelectrochemistry: fundamentals, experimental performance of PEM fuel cells. J. Electrochem. Soc. 159 (1), B53–B66. https://doi. techniques and applications. Wiley. WILEY. https://www.wiley.com/en-us/9780 org/10.1149/2.032201jes. 470843642. Degirmenci, U., Kirca, M., 2018. Design and mechanical characterization of a novel Bavykin, D.V., Passoni, L., Walsh, F.C., 2013. Hierarchical tube-in-tube structures carbon-based hybrid foam: A molecular dynamics study. Comput. Mater. Sci. 154, prepared by electrophoretic deposition of nanostructured titanates into a TiO2 122–131. https://doi.org/10.1016/j.commatsci.2018.06.039. nanotube array. Chem. Commun. 49 (62), 7007–7009. https://doi.org/10.1039/ Dekker, A., Heijne, A.T., Saakes, M., Hamelers, H.V., Buisman, C.J., 2009. Analysis and c3cc43264e. improvement of a scaled-up and stacked microbial fuel cell. Environ. Sci. Technol. Bhatia, S.K., Kim, J.H., Kim, M.S., Kim, J., Hong, J.W., Hong, Y.G., Kim, H.J., Jeon, J.M., 43 (23), 9038–9042. Kim, S.H., Ahn, J., Lee, H., Yang, Y.H., 2018. Production of (3-hydroxybutyrate-co-3- del Torno-de Román, L., Navarro, M., Hughes, G., Esquivel, J.P., Milton, R.D., Minteer, S. hydroxyhexanoate) copolymer from coffee waste oil using engineered Ralstonia D., Sabaté, N., 2018. Improved performance of a paper-based glucose fuel cell by eutropha. Bioprocess Biosyst. Eng. 41 (2), 229–235. https://doi.org/10.1007/ capillary induced flow. Electrochim. Acta 282, 336–342. https://doi.org/10.1016/j. s00449-017-1861-4. electacta.2018.05.074. Bhatt, P., Goe, A., 2017. Carbon Fibres: Production, properties and potential use. Mater. Deng, Y., Wheatley, A., 2016. Wastewater treatment in Chinese rural areas. Asian J. Sci. Res. India 14 (1), 52–57. https://doi.org/10.13005/msri/140109. Water Environ. Pollut. 13 (4), 1–11. Bird, H., Heidrich, E.S., Leicester, D.D., Theodosiou, P., 2022. Pilot-scale microbial fuel Dhibar, S., Das, C.K., 2014. Silver nanoparticles decorated polyaniline/multiwalled cells (MFCs): a meta-analysis study to inform full-scale design principles for carbon nanotubes nanocomposite for high-performance supercapacitor electrode. optimum wastewater treatment. J. Clean. Prod. 131227. Ind. Eng. Chem. Res. 53 (9), 3495–3508. https://doi.org/10.1021/ie402161e. Boodhoo, K.V.K., Flickinger, M.C., Woodley, J.M., Emanuelsson, E.A.C., 2022. Bioprocess Dietrich, K., Dumont, M.J., del Rio, L.F., Orsat, V., 2017. Producing PHAs in the intensification: a route to efficient and sustainable biocatalytic transformations for bioeconomy — towards a sustainable bioplastic. Sustain. Prod. Consump. 9, 58–70. the future. Chem. Eng. Process. Process Intensif. 108793 https://doi.org/10.1016/j. https://doi.org/10.1016/j.spc.2016.09.001. cep.2022.108793. Dincer, I., Acar, C., 2015. Review and evaluation of hydrogen production methods for Cai, M., Zhang, H., Zhang, Y., Wu, H., 2022. Bioelectrochemical assisted landfill better sustainability. Int. J. Hydrog. Energy 40 (34), 11094–11111. technology for the stabilization and valorization of food waste anaerobic digestate. Doyle, L.E., Marsili, E., 2018. Weak electricigens: a new avenue for bioelectrochemical Bioresour. Technol. 351, 126935 https://doi.org/10.1016/j.biortech.2022.126935. research. Bioresour. Technol. 258, 354–364. https://doi.org/10.1016/j. Callegari, A., Cecconet, D., Molognoni, D., Capodaglio, A.G., 2018. Sustainable biortech.2018.02.073. processing of dairy wastewater: long-term pilot application of a bio-electrochemical Dubey, R., Guruviah, V., 2019. Review of carbon-based electrode materials for system. J. Clean. Prod. 189, 563–569. https://doi.org/10.1016/j. supercapacitor energy storage. Ionics 25 (4), 1419–1445. https://doi.org/10.1007/ jclepro.2018.04.129. s11581-019-02874-0. Cambrian Innovation Inc, 2021. [WWW Document]. URL. https://www.cambrianinn E. U. W. Directive, 1991. Council Directive of 21. May 1991 concerning urban ovation.com/products/ecovolt (accessed 12.5.2022). wastewater treatment (91/271/EEC). Eur. J. Commun. 34, 40. Electro-active Technologies Inc.. [WWW Document]. URL. https://www.electroactive. tech/about-us (accessed 12.5.2022). 14 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Enzmann, F., Holtmann, D., 2019. Rational scale-up of a methane producing Hu, B., Harris, D.F., Dean, D.R., Liu, T.L., Yang, Z.Y., Seefeldt, L.C., 2018. Electrocatalytic bioelectrochemical reactor to 50 L pilot scale. Chem. Eng. Sci. 207, 1148–1158. CO2 reduction catalyzed by nitrogenase MoFe and FeFe proteins. https://doi.org/10.1016/j.ces.2019.07.051. Bioelectrochemistry 120, 104–109. https://doi.org/10.1016/j. EPA, E., 2001. Parameters of water quality interpretation and standards. Environmental bioelechem.2017.12.002. Protection Agency Ireland, Wexford, Ireland. Hu, K., Chen, W., Jia, S.Q., Wang, W., Han, F., 2019. Enhanced degradation of waste Escapa, A., Gil-Carrera, L., García, V., Morán, A., 2012. Performance of a continuous flow activated sludge in microbial electrolysis cell by ultrasonic treatment. Front. microbial electrolysis cell (MEC) fed with domestic wastewater. Bioresour. Technol. Microbiol. 128 https://doi.org/10.3389/fmicb.2019.00128. 117, 55–62. https://doi.org/10.1016/j.biortech.2012.04.060. Huong Le, T.X., Bechelany, M., Cretin, M., 2017. Carbon felt based-electrodes for energy European Commission, 2017, December. Report from the Commission to the European and environmental applications: a review. Carbon 122, 564–591. https://doi.org/ Parliament, the Council, the European Economic and Social Committee and the 10.1016/j.carbon.2017.06.078. Committee of the Regions, vol. No. 9. https://eur-lex.europa.eu/legal-content/en/ Hussain, S.A., Perrier, M., Tartakovsky, B., 2018. Long-term performance of a microbial ALL/?uri=CELEX:52017DC0749. electrolysis cell operated with periodic disconnection of power supply. RSC Adv. 8 Fattahi, M., Nabhani, N., Vaezi, M.R., Rahimi, E., 2011. Improvement of impact (30), 16842–16849. https://doi.org/10.1039/c8ra01863d. toughness of AWS E6010 weld metal by adding TiO2 nanoparticles to the electrode Ieropoulos, I.A., Greenman, J., Melhuish, C., Hart, J., 2005. Comparative study of three coating. Mater. Sci. Eng. A 528 (27), 8031–8039. https://doi.org/10.1016/j. types of microbial fuel cell. Enzym. Microb. Technol. 37 (2), 238–245. https://doi. msea.2011.07.035. org/10.1016/j.enzmictec.2005.03.006. Felseghi, R.A., Carcadea, E., Raboaca, M.S., Trufin, C.N., Filote, C., 2019. Hydrogen fuel Izadi, P., Fontmorin, J.M., Fernández, L.F., Cheng, S., Head, I., Yu, E.H., 2019. High cell technology for the sustainable future of stationary applications. Energies 12 performing gas diffusion biocathode for microbial fuel cells using acidophilic iron (23), 4593. oxidizing bacteria. Front. Energy Res. 93 https://doi.org/10.3389/ Field, J.A., Brady, J., 2003. Riboflavin as a redox mediator accelerating the reduction of fenrg.2019.00093. the azo dye Mordant Yellow 10 by anaerobic granular sludge. Water Sci. Technol. 48 Jadhav, D.A., Mungray, A.K., Arkatkar, A., Kumar, S.S., 2021. Recent advancement in (6), 187–193. scaling-up applications of microbial fuel cells: from reality to practicability. Sustain. Fitschen, J., Maly, M., Rosseburg, A., Wutz, J., Wucherpfennig, T., Schlüter, M., 2019. Energy Technol. Assess. 45, 101226. Influence of spacing of multiple impellers on power input in an industrial-scale Jadhav, D.A., Park, S.G., Pandit, S., Yang, E., Abdelkareem, M.A., Jang, J.K., Chae, K.J., aerated stirred tank reactor. Chemie Ingenieur Technik 91 (12), 1794–1801. 2022. Scalability of microbial electrochemical technologies: applications and Flint, S.H., Brooks, J.D., Bremer, P.J., 2000. Properties of the stainless steel substrate, challenges. Bioresour. Technol. 345, 126498. influencing the adhesion of thermo-resistant streptococci. J. Food Eng. 43, 235–242. Janicek, A., Fan, Y., Liu, H., 2014. Design of microbial fuel cells for practical application: Fu, Y., Liu, J., Su, J., Zhao, Z., Liu, Y., Xu, Q., 2012. Electrochemical properties of a review and analysis of scale-up studies. Biofuels 5 (1), 79–92. electrodes with different shapes and diffusion kinetic analysis of microbial fuel cells Jaouen, F., Morozan, A., 2014. Metal-organic frameworks: electrochemical properties. on ocean floor. J. Ocean Univ. China 11 (1), 25–31. https://doi.org/10.1007/ In: Encyclopedia of Inorganic and Bioinorganic Chemistry, pp. 1–24. https://doi. s11802-012-1808-y. org/10.1002/9781119951438.eibc2226. Gajdzik, J., Lenz, J., Natter, H., Walcarius, A., Kohring, G.W., Giffhorn, F., Göllü, M., Jeromiyas, N., Elaiyappillai, E., Kumar, A.S., Huang, S.T., Mani, V., 2019. Bismuth Demir, A.S., Hempelmann, R., 2012. Electrochemical screening of redox mediators nanoparticles decorated graphenated carbon nanotubes modified screen-printed for electrochemical regeneration of NADH. J. Electrochem. Soc. 159 (2), F10–F16. electrode for mercury detection. J. Taiwan Inst. Chem. Eng. 95, 466–474. https:// https://doi.org/10.1149/2.056202jes. doi.org/10.1016/j.jtice.2018.08.030. Galindo-de-la-Rosa, J., Vite-González, D., Díaz-Real, J.A., Vázquez-Maya, N., Álvarez, A., Jia, X., Li, M., Wang, Y., Wu, Y., Zhu, L., Wang, X., Zhao, Y., 2020. Enhancement of Arriaga, L.G., Ledesma-García, J., 2018, July. Alcohol dehydrogenase as bioanode hydrogen production and energy recovery through electro-fermentation from the for methanol and ethanol oxidation in a microfluidic fuel cell. J. Phys. Conf. Ser. vol. dark fermentation effluent of food waste. Environ. Sci. Ecotechnol. 1 (December 1052 (1), 012064. IOP Publishing. https://doi.org/10.1088/1742-6596/1052/1/0 2019), 100006 https://doi.org/10.1016/j.ese.2019.100006. 12064. Jones, A.K., Sillery, E., Albracht, S.P.J., Armstrong, F.A., 2002. Direct comparison of the Galindo-de-la-Rosa, J., Álvarez, A., Gurrola, M.P., Rodríguez-Morales, J.A., Oza, G., electrocatalytic oxidation of hydrogen by an enzyme and a platinum catalyst. Chem. Arriaga, L.G., Ledesma-García, J., 2020. Alcohol dehydrogenase immobilized on Commun. 2 (8), 866–867. https://doi.org/10.1039/b201337a. TiO2 nanotubes for ethanol microfluidic fuel cells. ACS Sustain. Chem. Eng. 8 (29), Jourdin, L., Burdyny, T., 2021. Microbial electrosynthesis: where do we go from here? 10900–10910. https://doi.org/10.1021/acssuschemeng.0c03219. Trends Biotechnol. 39 (4), 359–369. González-García, J., Frías, A., Expósito, E., Montiel, V., Aldaz, A., Conesa, J.A., 2000. Jugder, B.E., Welch, J., Aguey-Zinsou, K.F., Marquis, C.P., 2013. Fundamentals and Characterization of an electrochemical pilot-plant filter-press reactor by electrochemical applications of [Ni–Fe]-uptake hydrogenases. RSC Adv. 3 (22), hydrodynamic and mass transport studies. Ind. Eng. Chem. Res. 39 (5), 1132–1142. 8142–8159. https://doi.org/10.1039/C3RA22668A. https://doi.org/10.1021/ie990351q. Kadier, A., Simayi, Y., Abdeshahian, P., Azman, N.F., Chandrasekhar, K., Kalil, M.S., Grasemann, M., Laurenczy, G., 2012. Formic acid as a hydrogen source - recent 2016. A comprehensive review of microbial electrolysis cells (MEC) reactor designs developments and future trends. Energy Environ. Sci. 5 (8), 8171–8181. https://doi. and configurations for sustainable hydrogen gas production. Alex. Eng. J. 55 (1), org/10.1039/c2ee21928j. 427–443. https://doi.org/10.1016/j.aej.2015.10.008. Gude, V.G., 2016. Microbial fuel cells for wastewater treatment and energy generation. Kalathil, S., Patil, S.A., Pant, D., 2018. Microbial fuel cells: Electrode materials. In: In: Microbial Electrochemical and Fuel Cells: Fundamentals and Applications. Encyclopedia of Interfacial Chemistry: Surface Science and Electrochemistry (Issue Elsevier Ltd. https://doi.org/10.1016/B978-1-78242-375-1.00008-3 August). Elsevier Inc. https://doi.org/10.1016/B978-0-12-409547-2.13459-6 Haavisto, J.M., Kokko, M.E., Lay, C.H., Puhakka, J.A., 2017. Effect of hydraulic retention Kim, M.J., Seo, Y., Cruz, M.A., Wiley, B.J., 2019. Metal nanowire felt as a flow-through time on continuous electricity production from xylose in up-flow microbial fuel cell. electrode for high-productivity electrochemistry. ACS Nano 13 (6), 6998–7009. Int. J. Hydrog. Energy 42 (45), 27494–27501. https://doi.org/10.1021/acsnano.9b02058. Han, X., Wu, X., Deng, Y., Liu, J., Lu, J., Zhong, C., Hu, W., 2018. Ultrafine Pt Kochius, S., Magnusson, A.O., Hollmann, F., Schrader, J., Holtmann, D., 2012. nanoparticle-decorated pyrite-type CoS2 nanosheet arrays coated on carbon cloth as Immobilized redox mediators for electrochemical NAD(P)+ regeneration. Appl. a bifunctional electrode for overall water splitting. Adv. Energy Mater. 8 (24), 1–12. Microbiol. Biotechnol. 93 (6), 2251–2264. https://doi.org/10.1007/s00253-012- https://doi.org/10.1002/aenm.201800935. 3900-z. Harrington, T.D., Tran, V.N., Mohamed, A., Renslow, R., Biria, S., Orfe, L., Call, D.R., Kuk, S.K., Gopinath, K., Singh, R.K., Kim, T.D., Lee, Y., Choi, W.S., Lee, J., Park, C.B., Beyenal, H., 2015. The mechanism of neutral red-mediated microbial 2019. NADH-free electroenzymatic reduction of CO2 by conductive hydrogel- electrosynthesis in Escherichia coli: Menaquinone reduction. Bioresour. Technol. 192, conjugated formate dehydrogenase. ACS Catal. 9 (6), 5584–5589. https://doi.org/ 689–695. https://doi.org/10.1016/j.biortech.2015.06.037. 10.1021/acscatal.9b00127. Hendler, R.W., 1977. Automated electrodic potentiometry of potassium ferricyanide and Kumar, A., Hsu, L.H.H., Kavanagh, P., Barrière, F., Lens, P.N.L., Lapinsonnière, L., respiratory components. Anal. Chem. 49 (13), 1914–1918. https://doi.org/10.1021/ Lienhard, J.H., Schröder, U., Jiang, X., Leech, D., 2017. The ins and outs of ac50021a011. microorganism-electrode electron transfer reactions. Nat. Rev. Chem. 1, 1–13. Hengsbach, J.N., Sabel-Becker, B., Ulber, R., Holtmann, D., 2022. Microbial https://doi.org/10.1038/s41570-017-0024. electrosynthesis of methane and acetate—comparison of pure and mixed cultures. L.C.C. Aquacycl. [WWW Document]. URL. https://www.aquacycl.com/bett/ (accessed Appl. Microbiol. Biotechnol. 1–17. 12.5.2022). Hiegemann, H., Littfinski, T., Krimmler, S., Lübken, M., Klein, D., Schmelz, K.G., Li, J.H., Fu, Y. Bin, Liu, J., Li, A.L., Ma, D.D., 2009. Effect of electrode shape on power Ooms, K., Pant, D., Wichern, M., 2019. Performance and inorganic fouling of a and internal resistance in benthic microbial fuel cell material on marine sediment. submergible 255 L prototype microbial fuel cell module during continuous long-term Adv. Mater. Res. 79–82, 2195–2198. https://doi.org/10.4028/www.scientific.net/ operation with real municipal wastewater under practical conditions. Bioresour. AMR.79-82.2195. Technol. 294, 122227 https://doi.org/10.1016/j.biortech.2019.122227. Liao, P.Q., Shen, J.Q., Zhang, J.P., 2018. Metal–organic frameworks for electrocatalysis. Hirose, A., Kouzuma, A., Watanabe, K., 2019. Towards development of electrogenetics In: Coordination Chemistry Reviews, vol. 373. Elsevier B.V, pp. 22–48. https://doi. using electrochemically active bacteria. Biotechnol. Adv. 37 (6), 107351 https://doi. org/10.1016/j.ccr.2017.09.001. org/10.1016/j.biotechadv.2019.02.007. Lin, H.Y., Nurunnabi, M., Chen, W.H., Huang, C.H., 2019. Graphene in neuroscience. In: Hollmann, F., Hofstetter, K., Schmid, A., 2006. Non-enzymatic regeneration of Biomedical Applications of Graphene and 2D Nanomaterials, vol. Issue 12. Elsevier nicotinamide and flavin cofactors for monooxygenase catalysis. Trends Biotechnol. Inc. https://doi.org/10.1016/B978-0-12-815889-0.00016-7 24 (4), 163–171. https://doi.org/10.1016/j.tibtech.2006.02.003. Liu, P.S., Liang, K.M., 2000. Preparation and corresponding structure of nickel foam. Hou, B., Liu, X., Zhang, R., Li, Y., Liu, P., Lu, J., 2021. Investigation and evaluation of Mater. Sci. Technol. 16 (5), 575–578. https://doi.org/10.1179/ membrane fouling in a microbial fuel cell-membrane bioreactor systems (MFC- 026708300101508108. MBR). Sci. Total Environ. 152569 https://doi.org/10.1016/j. scitotenv.2021.152569. 15 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Liu, Y., Tay, J., 2001. Strategy for minimization of excess sludge production from the textile wastewater. Bioresour. Technol. 102 (2), 879–888. https://doi.org/10.1016/ activated sludge process. Biotechnol. Adv. 19 (2), 97–107. https://doi.org/10.1016/ j.biortech.2010.09.014. S0734-9750(00)00066-5. Olloqui-Sariego, J.L., Calvente, J.J., Andreu, R., 2021. Immobilizing redox enzymes at Liu, H., Ramnarayanan, R., Logan, B.E., 2004. Production of electricity during mesoporous and nanostructured electrodes. Curr. Opin. Electrochem. 26, 100658 wastewater treatment using a single chamber microbial fuel cell. Environ. Sci. https://doi.org/10.1016/j.coelec.2020.100658. Technol. 38 (7), 2281–2285. https://doi.org/10.1021/es034923g. Ottone, C., Lamberti, A., Fontana, M., Cauda, V., 2014a. Wetting behavior of hierarchical Liu, W., Huang, S., Zhou, A., Zhou, G., Ren, N., Wang, A., Zhuang, G., 2012. Hydrogen oxide nanostructures: TiO2 nanotubes from anodic oxidation decorated with ZnO generation in microbial electrolysis cell feeding with fermentation liquid of waste nanostructures. J. Electrochem. Soc. 161 (10), D484. https://doi.org/10.1149/ activated sludge. Int. J. Hydrog. Energy 37 (18), 13859–13864. https://doi.org/ 2.0431410jes. 10.1016/j.ijhydene.2012.04.090. Ottone, C., Laurenti, M., Motto, P., Stassi, S., Demarchi, D., Cauda, V.A., 2014b. ZnO Liu, Y., Li, F., Zhang, X., Ji, X., 2020a. Recent progress on electrochemical reduction of nanowires: Synthesis approaches and electrical properties. In: Nanowires. Synthesis, CO2 to methanol. Curr. Opin. Green Sustain. Chem. 23, 10–17. Electrical Properties and Uses in Biological Systems. Nova Publisher, New York, NY, Liu, W., Yang, G., Jia, H., Wang, J., 2020b. A novel UASB-MFC dual sensors system for USA, pp. 1–57. wastewater treatment: on-line sensor recovery and electrode cleaning in the long- Ottone, C., Hernández, S., Armandi, M., Bonelli, B., 2019. Scaling Up the Process of term operation. Chemosphere 246, 125751. https://doi.org/10.1016/j. Photo-Electrochemical Water Splitting. In: Testing Novel Water Oxidation Catalysts chemosphere.2019.125751. for Solar Fuels Production. Springer, Cham, pp. 93–114. https://doi.org/10.1007/ Lovley, D.R., 2011. Reach out and touch someone: Potential impact of DIET (direct 978-3-030-12712-1_6. interspecies energy transfer) on anaerobic biogeochemistry, bioremediation, and Ottone, C., Romero, O., Urrutia, P., Bernal, C., Illanes, A., Wilson, L., 2021a. Enzyme bioenergy. Rev. Environ. Sci. Biotechnol. 10 (2), 101–105. https://doi.org/10.1007/ biocatalysis and sustainability. In: Nanostructured Catalysts for Environmental s11157-011-9236-9. Applications. Springer, Cham, pp. 383–413. https://doi.org/10.1007/978-3-030- Lovley, D.R., 2017. Syntrophy goes electric: direct interspecies electron transfer. Annu. 58934-9_14. Rev. Microbiol. 71, 643–664. https://doi.org/10.1146/annurev-micro-030117- Ottone, C., Pugliese, D., Laurenti, M., Hernandez, S., Cauda, V., Grez, P., Wilson, L., 020420. 2021b. ZnO materials as effective anodes for the photoelectrochemical regeneration Lovley, D.R., Walker, D.J.F., 2019. Geobacter protein nanowires. Front. Microbiol. 10 of enzymatically active NAD+. ACS Appl. Mater. Interfaces 13 (9), 10719–10727. (September) https://doi.org/10.3389/fmicb.2019.02078. https://doi.org/10.1021/acsami.0c20630. Lu, Y., Koo, J., 2019. O2 sensitivity and H2 production activity of hydrogenases—a Pan, Y., Zhu, T., He, Z., 2019. Energy advantage of anode electrode rotation over anolyte review. Biotechnol. Bioeng. 116 (11), 3124–3135. https://doi.org/10.1002/ recirculation for operating a tubular microbial fuel cell. Electrochem. Commun. 106, bit.27136. 106529. Lu, L., Xing, D., Liu, B., Ren, N., 2012. Enhanced hydrogen production from waste Papillon, J., Ondel, O., Maire, É., 2021. Scale up of single-chamber microbial fuel cells activated sludge by cascade utilization of organic matter in microbial electrolysis with stainless steel 3D anode: Effect of electrode surface areas and electrode spacing. cells. Water Res. 46 (4), 1015–1026. https://doi.org/10.1016/j.watres.2011.11.073. Bioresource Technol. Rep. 13, 100632. Maria, I.S.M., Raul, M., Begona, C., Adrian, E., Antonio, M., 2018. Pilot-scale Patel, D., Bapodra, S.L., Madamwar, D., Desai, C., 2021. Electroactive bacterial bioelectrochemical system for simultaneous nitrogen and carbon removal in urban community augmentation enhances the performance of a pilot scale constructed wastewater treatment plants. J. Biosci. Bioeng. 126 (6), 758–763. https://doi.org/ wetland microbial fuel cell for treatment of textile dye wastewater. Bioresour. 10.1016/j.jbiosc.2018.06.008. Technol. 332, 125088 https://doi.org/10.1016/j.biortech.2021.125088. Martinez, C.M., Alvarez, L.H., 2018. Application of redox mediators in Peng, H.Y., Wang, N., Zheng, Y.F., Lifshitz, Y., Kulik, J., Zhang, R.Q., Lee, C.S., Lee, S.T., bioelectrochemical systems. Biotechnol. Adv. 36 (5), 1412–1423. https://doi.org/ 2000. Smallest diameter carbon nanotubes. Appl. Phys. Lett. 77 (18), 2831–2833. 10.1016/j.biotechadv.2018.05.005. https://doi.org/10.1063/1.1320869. Meckstroth, M.L., Norris, B.J., Heineman, W.R., 1981. 387 — Mediator-titrants for thin- Petroll, K., Kopp, D., Care, A., Bergquist, P.L., Sunna, A., 2019. Tools and strategies for layer spectroelectrochemical measurement of biocomponent Uo and n values. constructing cell-free enzyme pathways. Biotechnol. Adv. 37 (1), 91–108. ′ Bioelectrochem. Bioenerg. 8 (1), 63–70. https://doi.org/10.1016/0302-4598(81) Pham, T.H., Boon, N., Aelterman, P., Clauwaert, P., de Schamphelaire, L., Vanhaecke, L., 85007-6. de Maeyer, K., Höfte, M., Verstraete, W., Rabaey, K., 2008. Metabolites produced by Microorganic Technologies Inc. [WWW Document]. URL. https://www.microrganictech. Pseudomonas sp. enable a Gram-positive bacterium to achieve extracellular electron com/viva (accessed 12.5.2022). transfer. Appl. Microbiol. Biotechnol. 77 (5), 1119–1129. https://doi.org/10.1007/ Milton, R.D., Minteer, S.D., 2019. Nitrogenase bioelectrochemistry for synthesis s00253-007-1248-6. applications. Acc. Chem. Res. 52 (12), 3351–3360. https://doi.org/10.1021/acs. Pietricola, G., Ottone, C., Fino, D., Tommasi, T., 2020. Enzymatic reduction of CO2 to accounts.9b00494. formic acid using FDH immobilized on natural zeolite. J. CO2 Utiliz. 42, 101343 Mohamed, S.N., Hiraman, P.A., Muthukumar, K., Jayabalan, T., 2020. Bioelectricity https://doi.org/10.1016/j.jcou.2020.101343. production from kitchen wastewater using microbial fuel cell with photosynthetic Pietricola, G., Tommasi, T., Dosa, M., Camelin, E., Berruto, E., Ottone, C., Fino, D., algal cathode. Bioresour. Technol. 295, 122226 https://doi.org/10.1016/j. Cauda, V., Piumetti, M., 2021. Synthesis and characterization of ordered mesoporous biortech.2019.12222. silicas for the immobilization of formate dehydrogenase (FDH). Int. J. Biol. Mohan, S.V., Velvizhi, G., Modestra, J.A., Srikanth, S., 2014. Microbial fuel cell: critical Macromol. 177, 261–270. https://doi.org/10.1016/j.ijbiomac.2021.02.114. factors regulating bio-catalyzed electrochemical process and recent advancements. Pietricola, G., Chamorro, L., Castellino, M., Maureira, D., Tommasi, T., Hernández, S., Renew. Sust. Energ. Rev. 40, 779–797. https://doi.org/10.1016/j.rser.2014.07.109. Ottone, C., 2022. Covalent immobilization of dehydrogenases on carbon felt for Mohanakrishna, G., Kondaveeti, S., Desale, P., el Mekawy, A., Abu-Reesh, I.M., 2018. reusable anodes with effective electrochemical cofactor regeneration. Enzymatic electrosynthesis toward value addition. In: Biomass, Biofuels, ChemistryOpen 11 (11), e202200102. Biochemicals: Microbial Electrochemical Technology: Sustainable Platform for Fuels, Plant-e. [WWW Document]. URL. https://www.plant-e.com/en/producten/ (accessed Chemicals and Remediation. Elsevier B.V. https://doi.org/10.1016/B978-0-444- 12.5.2022). 64052-9.00039-X. Qadir, M., Drechsel, P., Jiménez Cisneros, B., Kim, Y., Pramanik, A., Mehta, P., Montillet, A., Comiti, J., Legrand, J., 1994. Application of metallic foams in Olaniyan, O., 2020. February. Global and regional potential of wastewater as a electrochemical reactors of the filter-press type: Part II Mass transfer performance. water, nutrient and energy source. In: Natural resources forum. Blackwell Publishing J. Appl. Electrochem. 24 (5), 384–389. https://doi.org/10.1007/BF00254149. Ltd., Oxford, UK, pp. 40–51. https://doi.org/10.1111/1477-8947.12187. Vol. 44, Motabar, D., Li, J., Payne, G.F., Bentley, W.E., 2021. Mediated electrochemistry for No. 1. redox-based biological targeting: entangling sensing and actuation for maximizing Quinn, B.M., Dekker, C., Lemay, S.G., 2005. Electrodeposition of noble metal information transfer. Curr. Opin. Biotechnol. 71, 137–144. https://doi.org/10.1016/ nanoparticles on carbon nanotubes. J. Am. Chem. Soc. 127 (17), 6146–6147. j.copbio.2021.07.017. https://doi.org/10.1021/ja0508828. Muddemann, T., Haupt, D., Sievers, M., Kunz, U., 2019. Electrochemical reactors for Qyyum, M.A., Ihsanullah, I., Ahmad, R., Ismail, S., Khan, A., Nizami, A.S., Tawfik, A., wastewater treatment. ChemBioEng Rev. 6 (5), 142–156. https://doi.org/10.1002/ 2022. Biohydrogen production from real industrial wastewater: Potential cben.201900021. bioreactors, challenges in commercialization and future directions. Int. J. Hydrog. Nagendranatha Reddy, C., Sudhakar, M.P., Min, B., Shanmugam, P., 2018. In: Energy. 47, 37154–37170. Sivasankar, V., Mylsamy, P., Omine, K. (Eds.), Microbial Fuel Cell Technology for Radhakrishnan, V., Haridoss, P., 2011. Differences in structure and property of carbon Bioelectricity. Springer International Publishing. https://doi.org/10.1007/978-3- paper and carbon cloth diffusion media and their impact on proton exchange 319-92904-0. membrane fuel cell flow field design. Mater. Des. 32 (2), 861–868. https://doi.org/ Nakhate, P.H., Patil, H.G., Shah, V., Salvi, T., Marathe, K.V., 2019. Process validation of 10.1016/j.matdes.2010.07.009. integrated bioelectrochemical and membrane reactor for synchronous bioenergy Rahimnejad, M., Najafpour, G.D., Ghoreyshi, A.A., Shakeri, M., Zare, H., 2011. extraction and sustainable wastewater treatment at a semi-pilot scale. Biochem. Eng. Methylene blue as electron promoters in microbial fuel cell. Int. J. Hydrog. Energy J. 151, 107309 https://doi.org/10.1016/j.bej.2019.107309. 36 (20), 13335–13341. https://doi.org/10.1016/j.ijhydene.2011.07.059. Nath, D., Ghangrekar, M.M., 2020. Plant secondary metabolites induced electron flux in Ren, S., Wang, Z., Bilal, M., Feng, Y., Jiang, Y., Jia, S., Cui, J., 2020. Co-immobilization microbial fuel cell: investigation from laboratory-to-field scale. Sci. Rep. 10 (1), multienzyme nanoreactor with co-factor regeneration for conversion of CO2. Int. J. 1–17. https://doi.org/10.1038/s41598-020-74092-y. Biol. Macromol. 155, 110–118. https://doi.org/10.1016/j.ijbiomac.2020.03.177. Nishio, K., Kimoto, Y., Song, J., Konno, T., Ishihara, K., Kato, S., Hashimoto, K., Rengaraj, S., Kavanagh, P., Leech, D., 2011. Biosensors and bioelectronics: A comparison Nakanishi, S., 2013. Extracellular electron transfer enhances polyhydroxybutyrate of redox polymer and enzyme co-immobilization on carbon electrodes to provide productivity in Ralstonia eutropha. Environ. Sci. Technol. Lett. 1 (1), 40–43. https:// membrane-less glucose / O2 enzymatic fuel cells with improved power output and doi.org/10.1021/ez400085b. stability. Biosens. Bioelectron. 30 (1), 294–299. https://doi.org/10.1016/j. Novotný, Č., Svobodová, K., Benada, O., Kofroňová, O., Heissenberger, A., Fuchs, W., bios.2011.09.032. 2011. Potential of combined fungal and bacterial treatment for color removal in 16 D. Maureira et al. Biotechnology Advances 64 (2023) 108123 Rossi, R., Logan, B.E., 2022. Impact of reactor configuration on pilot-scale microbial fuel Vaghari, H., Jafarizadeh-Malmiri, H., Mohammadlou, M., Berenjian, A., Anarjan, N., cell performance. Water Res. 119179. Jafari, N., Nasiri, S., 2016. Application of magnetic nanoparticles in smart enzyme Rossi, R., Hur, A.Y., Page, M.A., Thomas, A.O.B., Butkiewicz, J.J., Jones, D.W., Baek, G., immobilization. Biotechnol. Lett. 38 (2), 223–233. https://doi.org/10.1007/s10529- Saikaly, P.E., Cropek, D.M., Logan, B.E., 2022. Pilot scale microbial fuel cells using 015-1977-z. air cathodes for producing electricity while treating wastewater. Water Res. 215, Verbeeck, K., Gildemyn, S., Rabaey, K., 2018. Membrane electrolysis assisted gas 118208 https://doi.org/10.1016/j.watres.2022.118208. fermentation for enhanced acetic acid production. Front. Energy Res. 6, 88. https:// Rozendal, R.A., Hamelers, H.V., Rabaey, K., Keller, J., Buisman, C.J., 2008. Towards doi.org/10.3389/fenrg.2018.00098. practical implementation of bioelectrochemical wastewater treatment. Trends Vignais, P., Billoud, B., Meyer, J., 2001. Classification and phylogeny of hydrogenases. Biotechnol. 26 (8), 450–459. https://doi.org/10.1016/j.tibtech.2008.04.008. FEMS Microbiol. Rev. 25, 455–501. https://doi.org/10.1111/j.1574-6976.2001. Sakkos, J.K., Wackett, L.P., Aksan, A., 2019. Enhancement of biocatalyst activity and tb00587.x. protection against stressors using a microbial exoskeleton. Sci. Rep. 9 (1), 1–12. Vikrant, K., Kumar, V., Kim, K.H., Kukkar, D., 2017. Metal-organic frameworks (MOFs): https://doi.org/10.1038/s41598-019-40113-8. Potential and challenges for capture and abatement of ammonia. J. Mater. Chem. A 5 Samrat, M.N., Rao, K.K., Ruggeri, B., Tommasi, T., 2018. Denitrification of water in a (44), 22877–22896. https://doi.org/10.1039/c7ta07847a. microbial fuel cell (MFC) using seawater bacteria. J. Clean. Prod. 178, 449–456. Waller, M.G., Trabold, T.A., 2013, July. Review of microbial fuel cells for wastewater San-Martín, M.I., Sotres, A., Alonso, R.M., Díaz-Marcos, J., Morán, A., Escapa, A., 2019. treatment: large-scale applications, future needs and current research gaps. In: Assessing anodic microbial populations and membrane ageing in a pilot microbial International Conference on Fuel Cell Science, Engineering and Technology, vol. electrolysis cell. Int. J. Hydrog. Energy 44 (32), 17304–17315. https://doi.org/ 55522. American Society of Mechanical Engineers. https://doi.org/10.1115/ 10.1016/j.ijhydene.2019.01.287. FuelCell2013-18185. V001T01A011. Savla, N., Pandit, S., Verma, J.P., Awasthi, A.K., Sana, S.S., Prasad, R., 2021. Techno- Walsh, F.C., Arenas, L.F., Ponce de León, C., Reade, G.W., Whyte, I., Mellor, B.G., 2016. economical evaluation and life cycle assessment of microbial electrochemical The continued development of reticulated vitreous carbon as a versatile electrode systems: a review. Curr. Res. Green Sustain. Chem. 4, 100111. material: Structure, properties and applications. Electrochim. Acta 215, 566–591. Selvaraj, D., Velvizhi, G., 2023. Self-sustained semi-pilot scale hybrid eco-electrogenic https://doi.org/10.1016/j.electacta.2016.08.103. engineered system for the wastewater treatment and bioenergy generation. J. Water Walter, X.A., Forbes, S., Greenman, J., Ieropoulos, I.A., 2016. From single MFC to Process. Eng. 51, 103474. https://doi.org/10.1016/j.jwpe.2022.103474. cascade configuration: the relationship between size, hydraulic retention time and Sen, S., Liu, D., Palmore, G.T.R., 2014. Electrochemical reduction of CO2 at copper power density. Sustain. Energy Technol. Assess. 14, 74–79. nanofoams. ACS Catal. 4 (9), 3091–3095. https://doi.org/10.1021/cs500522g. Wang, S.F., Xie, F., Hu, R.F., 2007. Carbon-coated nickel magnetic nanoparticles Sevda, S., Sreekrishnan, T.R., 2012. Effect of salt concentration and mediators in salt modified electrodes as a sensor for determination of acetaminophen. Sensors bridge microbial fuel cell for electricity generation from synthetic wastewater. Actuators B Chem. 123 (1), 495–500. https://doi.org/10.1016/j.snb.2006.09.031. J. Environ. Sci. Health A Tox. Haz. Subst. Environ. Eng. 47 (6), 878–886. https://doi. Wang, Y., Wei, H., Lu, Y., Wei, S., Wujcik, E.K., Guo, Z., 2015. Multifunctional carbon org/10.1080/10934529.2012.665004. nanostructures for advanced energy storage applications. Nanomaterials 5 (2), Sindhuja, M., Harinipriya, S., Bala, A.C., Ray, A.K., 2018. Environmentally available 755–777. https://doi.org/10.3390/nano5020755. biowastes as substrate in microbial fuel cell for efficient chromium reduction. Whitehead, K.A., Verran, J., 2006. The effect of surface topography on the retention of J. Hazard. Mater. 355, 197–205. https://doi.org/10.1016/j.jhazmat.2018.05.030. microorganisms. Food Bioprod. Process. 84 (4 C), 253–259. https://doi.org/ Su, X., Xu, J., Liang, B., Duan, H., Hou, B., Huang, Y., 2016. Catalytic carbon dioxide 10.1205/fbp06035. hydrogenation to methane: a review of recent studies. J. Energy Chem. 25 (4), Xia, H., Hong, C., Shi, X., Li, B., Yuan, G., Yao, Q., Xie, J., 2015. Hierarchical 553–565. https://doi.org/10.1016/j.jechem.2016.03.009. heterostructures of Ag nanoparticles decorated MnO2 nanowires as promising Sulaymon, A.H., Abbar, A.H., 2012. Scale-up of electrochemical reactors. Electrolysis 17. electrodes for supercapacitors. J. Mater. Chem. A 3 (3), 1216–1221. https://doi.org/ https://doi.org/10.5772/48728. 10.1039/c4ta05568c. Suransh, J., Jadhav, D.A., Nguyen, D.D., Mungray, A.K., 2023. Scalable architecture of Yang, X., 2010. Scale-Up of Microbial Fermentation Process. Man. Indus. Microbiol. low-cost household microbial fuel cell for domestic wastewater treatment and Biotechnol. 669–675. simultaneous energy recovery. Sci. Total Environ. 857, 159671 https://doi.org/ Ye, Y., Ngo, H.H., Guo, W., Chang, S.W., Nguyen, D.D., Zhang, X., Liu, Y., 2020. Impacts 10.1016/j.scitotenv.2022.159671. of hydraulic retention time on a continuous flow mode dual-chamber microbial fuel Tahir, K., Miran, W., Jang, J., Woo, S.H., Lee, D.S., 2021. Enhanced product selectivity in cell for recovering nutrients from municipal wastewater. Sci. Total Environ. 734, the microbial electrosynthesis of butyrate using a nickel ferrite-coated biocathode. 139220. Environ. Res. 196, 110907. Yuan, M., Sahin, S., Cai, R., Abdellaoui, S., Hickey, D.P., Minteer, S.D., Milton, R.D., Tamirat, A.G., Guan, X., Liu, J., Luo, J., Xia, Y., 2020. Redox mediators as charge agents 2018. Creating a low-potential redox polymer for efficient electroenzymatic CO2 for changing electrochemical reactions. Chem. Soc. Rev. 49 (20), 7454–7478. reduction. Angew. Chem. 130 (22), 6692–6696. https://doi.org/10.1002/ https://doi.org/10.1039/d0cs00489h. anie.201803397. Terzi, F., Pigani, L., Zanardi, C., 2019. Unusual metals as electrode materials for Zeppilli, M., Cristiani, L., Dell’Armi, E., Majone, M., 2020. Bioelectromethanogenesis electrochemical sensors. Curr. Opin. Electrochem. 16, 157–163. https://doi.org/ reaction in a tubular Microbial Electrolysis Cell (MEC) for biogas upgrading. Renew. 10.1016/j.coelec.2019.05.005. Energy 158, 23–31. https://doi.org/10.1016/j.renene.2020.05.122. Thamilselvan, A., Nesaraj, A.S., Noel, M., 2016. Review on carbon-based electrode Zhang, Z., Li, J., Ji, M., Liu, Y., Wang, N., Zhang, X., Zhang, S., Ji, X., 2021. materials for application in capacitive deionization process. Int. J. Environ. Sci. Encapsulation of multiple enzymes in a metal–organic framework with enhanced Technol. 13 (12), 2961–2976. https://doi.org/10.1007/s13762-016-1061-9. electro-enzymatic reduction of CO2 to methanol. Green Chem. 23 (6), 2362–2371. Thiele, B., Rieder, O., Jehmlich, N., von Bergen, M., Müller, M., Boll, M., 2008. Zhang, Z., Sarkar, D., Li, L., Datta, R., 2022. Contaminant removal and resource recovery Aromatizing cyclohexa-1,5-diene-1-carbonyl-coenzyme A oxidase: Characterization in bioelectrochemical wastewater treatment. Curr. Pollut. Rep. 1-18 https://doi.org/ and its role in anaerobic aromatic metabolism. J. Biol. Chem. 283 (30), 10.1007/s40726-022-00218-7. 20713–20721. https://doi.org/10.1074/jbc.M802841200. Zhao, F., Slade, R.C.T., Varcoe, J.R., 2009. Techniques for the study and development of Tian, J.H., Lacroix, R., Yaqoob, A.A., Bureau, C., Midoux, C., Desmond-Le Quéméner, E., microbial fuel cells: An electrochemical perspective. Chem. Soc. Rev. 38 (7), Bouchez, T., 2023. Study of a pilot scale microbial electrosynthesis reactor for 1926–1939. https://doi.org/10.1039/b819866g. organic waste biorefinery. Energies 16 (2), 591. https://doi.org/10.3390/ Zhao, Y., Ding, Y., Li, Y., Peng, L., Byon, H.R., Goodenough, J.B., Yu, G., 2015. en16020591. A chemistry and material perspective on lithium redox flow batteries towards high- Tiquia-Arashiro, S.M., 2020. Electricity Production from Carbon Monoxide and Syngas in density electrical energy storage. Chem. Soc. Rev. 44 (22), 7968–7996. https://doi. a Thermophilic Microbial Fuel Cell. Microbial Electrochemical Technologies org/10.1039/C5CS00289C. 288–299. Zheng, T., Li, J., Ji, Y., Zhang, W., Fang, Y., Xin, F., Weiliang, D., Ping, W., Jiangfeng, M., Tomassetti, M., Angeloni, R., Marchiandi, S., Castrucci, M., Martini, E., Campanella, L., 2020. Progress and prospects of bioelectrochemical systems: electron transfer and its 2020. Direct methanol catalytic fuel cell, for measuring ethanol contents in applications in the microbial metabolism. Front. Bioeng. Biotechnol. 10 https://doi. pharmaceutical tinctures. Curr. Anal. Chem. 16 (2), 184–194. org/10.3389/fbioe.2020.00010. Tsujimura, S., Tatsumi, H., Ogawa, J., Shimizu, S., Kano, K., Ikeda, T., 2001. Zhou, M., Chi, M., Luo, J., He, H., Jin, T., 2011. An overview of electrode materials in Bioelectrocatalytic reduction of dioxygen to water at neutral pH using bilirubin microbial fuel cells. J. Power Sources 196 (10), 4427–4435. https://doi.org/ oxidase as an enzyme and 2,2′ -azinobis (3-ethylbenzothiazolin-6-sulfonate) as an 10.1016/j.jpowsour.2011.01.012. electron transfer mediator. J. Electroanal. Chem. 496 (1–2), 69–75. https://doi.org/ 10.1016/S0022-0728(00)00239-4. 17