Microbial | electrochemical CO2 reduction: To integrate or not to integrate?

Abstract

Paniz Izadi is a lead scientist for the H2020-funded project VIVALDI at Helmholtz-Centre for Environmental Research (UFZ), Germany. Her current research focuses on developing methods for electrochemical CO2 reduction and its interfacing to microbiology for industrial applications, following her previous research on microbial CO2 reduction in bio-electrochemical systems. She received her PhD in chemical engineering from Newcastle University, UK in 2020.Falk Harnisch holds a full professorship at Leipzig University for electrobiotechnology and is a group leader at the Helmholtz-Centre for Environmental Research (UFZ), Germany. He received his PhD from Greifswald University, Germany in 2009, as well as several fellowships and awards, and is currently serving as a president of the International Society for Microbial Electrochemistry and Technology. His research ranges from fundamentals of microbial electrochemistry via electro-organic synthesis to engineering of microbial electrochemical technologies. Paniz Izadi is a lead scientist for the H2020-funded project VIVALDI at Helmholtz-Centre for Environmental Research (UFZ), Germany. Her current research focuses on developing methods for electrochemical CO2 reduction and its interfacing to microbiology for industrial applications, following her previous research on microbial CO2 reduction in bio-electrochemical systems. She received her PhD in chemical engineering from Newcastle University, UK in 2020. Falk Harnisch holds a full professorship at Leipzig University for electrobiotechnology and is a group leader at the Helmholtz-Centre for Environmental Research (UFZ), Germany. He received his PhD from Greifswald University, Germany in 2009, as well as several fellowships and awards, and is currently serving as a president of the International Society for Microbial Electrochemistry and Technology. His research ranges from fundamentals of microbial electrochemistry via electro-organic synthesis to engineering of microbial electrochemical technologies. Carbon dioxide (CO2) must turn from waste to feedstock in order to establish a circular economy. Although there is consensus that chemicals and fuels for consumer goods will be based on the carbon that was recently CO2, one can only make inferences regarding the technology platform(s) that will be needed to reach such an industrial transformation. Certainly, the current petro-based industries will not be simply replaced by one technology. Rather, a broad portfolio of platforms comprised of physical, chemical and biological technologies can be expected in order to allow development toward a true circularity of (bio)chemical synthesis. Among these technologies are platforms based on interweaving microbial and electrochemical synthesis.1Harnisch F. Urban C. Electrobiorefineries: unlocking the synergy of electrochemical and microbial conversions.Angew. Chem. Int. Edition. 2018; 57: 10016-10023https://doi.org/10.1002/anie.201711727Crossref PubMed Scopus (43) Google Scholar Microbial synthesis based on the immediate utilization of CO2 as a feedstock in gas fermentation, for instance, suffers from low solubility of gaseous compounds in their liquid phase. It limits the accessibility of CO2 and/or H2 for microbial cells and therefore limits conversion efficiency.2Vees C.A. Neuendorf C.S. Pflügl S. Towards continuous industrial bioprocessing with solventogenic and acetogenic clostridia: challenges, progress and perspectives.J. Ind. Microbiol. Biotechnol. Official J. Soc. Ind. Microbiol. Biotechnol. 2020; 47: 753-787https://doi.org/10.1007/s10295-020-02296-2Crossref PubMed Scopus (21) Google Scholar Electrochemistry allows the use of electric and not chemical energy to exploit CO2 for synthesis; however, the electrochemical CO2-reduction reaction (CO2RR) is characterized by its low product portfolio that is commonly limited to C1 or C2 compounds3Nitopi S. Bertheussen E. Scott S.B. Liu X. Engstfeld A.K. Horch S. Seger B. Stephens I.E.L. Chan K. Hahn C. et al.Progress and perspectives of electrochemical CO2 reduction on copper in aqueous electrolyte.Chem. Rev. 2019; 119: 7610-7672https://doi.org/10.1021/acs.chemrev.8b00705Crossref PubMed Scopus (1218) Google Scholar but possesses high kinetics, particularly when compared to biological CO2 reduction.4Hegner R. Rosa L.F. Harnisch F. Electrochemical CO2 reduction to formate at indium electrodes with high efficiency and selectivity in pH neutral electrolytes.Appl. Catal. B: Environ. 2018; 238: 546-556https://doi.org/10.1016/j.apcatb.2018.07.030Crossref Scopus (56) Google Scholar Therefore, combining or integrating microbial conversions with CO2RR for synthesis seems very appealing. Integration may allow harnessing the best of both systems utilizing electric energy and CO2 in order to create a broad portfolio of products. Microbial electrochemical synthesis (MES) is based on interfacing electrochemical and microbial transformations to allow the purposeful transformation of a feedstock into a desired product.1Harnisch F. Urban C. Electrobiorefineries: unlocking the synergy of electrochemical and microbial conversions.Angew. Chem. Int. Edition. 2018; 57: 10016-10023https://doi.org/10.1002/anie.201711727Crossref PubMed Scopus (43) Google Scholar MES can be based on the activity of autotrophic microorganisms that reduce CO2 using cathodic electrons or hydrogen. Despite initial excitement regarding this process and significant research on MES from CO2, its development has stagnated and seems to face insurmountable hurdles. The main obstacles are limited electron transfer rates and hence reaction rates, limited product portfolio, and insufficient yields, as well as a long amount of time required for developing a cathodic microbial electrocatalyst and therefore a long production start-up time.5Prévoteau A. Carvajal-Arroyo J.M. Ganigué R. Rabaey K. Microbial electrosynthesis from CO2: forever a promise?.Curr. Opin. Biotechnol. 2020; 62: 48-57https://doi.org/10.1016/j.copbio.2019.08.014Crossref PubMed Scopus (124) Google Scholar Synthesis from CO2 can also be based on less immediate interfacing of microbial and electrochemical reactions. Through CO2RR, CO2 is first electrochemically reduced to yield formate (HCOOH) or other C1 compounds, which are already established feedstocks for microbial syntheses. Therefore, one can foresee that in addition to using formatotrophs (formate-consuming microorganisms) for synthesis, strain engineering will make formate an excellent feedstock for several production hosts, including yeasts.6Cotton C.A. Claassens N.J. Benito-Vaquerizo S. Bar-Even A. Renewable methanol and formate as microbial feedstocks.Curr. Opin. Biotechnol. 2020; 62: 168-180https://doi.org/10.1016/j.copbio.2019.10.002Crossref PubMed Scopus (98) Google Scholar Integration of CO2RR that yields formate with microbial synthesis from formate was first reported by Li et al.7Li H. Opgenorth P.H. Wernick D.G. Rogers S. Wu T.-Y. Higashide W. Malati P. Huo Y.-X. Cho K.M. Liao J.C. Integrated electromicrobial conversion of CO2 to higher alcohols.Science. 2012; 335: 1596https://doi.org/10.1126/science.1217643Crossref PubMed Scopus (465) Google Scholar Since then, a significant development has taken place that concerns electrochemical and microbial engineering of components, as well as process engineering. When integrating CO2RR and microbial synthesis, different approaches are feasible. The integration can occur in situ, that is, in one compartment (Figure 1A ). CO2 is converted into formate by CO2RR proceeding at the cathode and is linked to synthesis by microorganisms. Here, the synchronization of the CO2RR and microbial synthesis rates is a challenge. To avoid disturbing CO2RR at the electrode, microorganisms that form no biofilm thereon are favorable. The submersed microorganisms are also more appealing in terms of volumetric production rates and yields, especially when exploiting co-cultures of different microorganisms, which allows the creation of food webs for gaining complex products. It is noteworthy that often the main or only electrochemical side product is H2, which is an ideal energy source for many microbial catalysts. Alternatively, the process of CO2RR yielding formate occurs while being separated spatially from microbial synthesis (Figures 1B and 1C). The solution composition can be critical, as it needs to balance the requirements of both process steps and thus provide (optimal) conditions for CO2RR and microbial synthesis. A challenge can be the inhibition of CO2RR by bio-products. Using two separate reactors (Figure 1B), including inline separation of the microbial products and reusing the solution for CO2RR, can overcome this problem. Solution design can be especially challenging as some compounds that are vital for microbial growth or a pH required for microbial growth and activity can hamper CO2RR.4Hegner R. Rosa L.F. Harnisch F. Electrochemical CO2 reduction to formate at indium electrodes with high efficiency and selectivity in pH neutral electrolytes.Appl. Catal. B: Environ. 2018; 238: 546-556https://doi.org/10.1016/j.apcatb.2018.07.030Crossref Scopus (56) Google Scholar In this line, the purity of the gaseous CO2 feed is also of relevance—for instance, when assuming that an industrial feed of flue gas contains impurities (e.g. traces of O2 or sulfur compounds). As well as chemical compounds, biomass can be detrimental for CO2RR when present at the electrode and can be affected by the electrochemical reaction. Thus, biomass removal, e.g., filtering, is advantageous when integrating separate reactors. In addition, a small share of impurities (e.g., O2) in the feed gas can be tolerated by CO2RR. We are confident that engineering allows us to balance the operational conditions for CO2RR and microbial synthesis as required; however, controlling operational conditions such as pH for integrated processes remains challenging. Alternatively, the electrochemical and biological reactions can be fully separated (Figure 1C). This separation allows decoupling two process steps in space and time. As CO2RR and microbial synthesis are fully independent, they do not affect each other, and the solutions can be optimized for the respective process step. Further, separating them allows concentration as well as amendment—for instance, with trace elements—of the solution containing CO2RR products before supplying it to a bioreactor. The rate of CO2RR and microbial synthesis can be disconnected in time when both are fully spatially separated (Figure 1C), whereas only a integration requires synchronization to some extent (Figure 1B), and particularly full synchronization is required when operating in one compartment (Figure 1A). At first glance, separated processes may be even more advantageous by allowing precise control of the feeding of formate to the bioreactor. This is particularly advantageous, as high formate concentration can be toxic, as can high concentration of the bio-products. The latter can be removed using downstream processing (DSP). Although the toxicity threshold of formate is different (ranging from <100 mM for weak formate dehydrogenases [e.g. E.coli] to >100 mM for those with strong [e.g. yeasts] formate dehydrogenases), a higher concentration than the threshold causes decline of biosynthesis.6Cotton C.A. Claassens N.J. Benito-Vaquerizo S. Bar-Even A. Renewable methanol and formate as microbial feedstocks.Curr. Opin. Biotechnol. 2020; 62: 168-180https://doi.org/10.1016/j.copbio.2019.10.002Crossref PubMed Scopus (98) Google Scholar However, when using locally separated process steps (Figures 1B and 1C), concentration gradients in the bioreactor already limit the microbial synthesis. This requires improved mass transfer, such as increased energy-consuming agitation or implementation of baffles.8Liew F. Martin M.E. Tappel R.C. Heijstra B.D. Mihalcea C. Köpke M. Gas fermentation—a flexible platform for commercial scale production of low-carbon-fuels and chemicals from waste and renewable feedstocks.Front. Microbiol. 2016; 7: 694https://doi.org/10.3389/fmicb.2016.00694Crossref PubMed Scopus (229) Google Scholar We argue that this limitation can be elegantly and economically overcome by using an appropriate electrode and reactor design for in situ integration, e.g., implementation of three-dimensional electrodes as discussed below. We are confident that the above illustrated integration can become economically competitive, with its main assets being the fact that the kinetics of CO2RR lead to a low ratio of the needed active electrode surface area to reactor volume and the product diversity of microbial synthesis. The main competitor will be gas fermentation from syngas (from CO/H2O or CO2/H2). However, the solubility of gaseous feedstock is limited (e.g., 28 mg L−1 CO, 1.6 mg L−1 H2, and 1.7 g L−1 CO2; 293K; and 1atm8Liew F. Martin M.E. Tappel R.C. Heijstra B.D. Mihalcea C. Köpke M. Gas fermentation—a flexible platform for commercial scale production of low-carbon-fuels and chemicals from waste and renewable feedstocks.Front. Microbiol. 2016; 7: 694https://doi.org/10.3389/fmicb.2016.00694Crossref PubMed Scopus (229) Google Scholar) and therefore sets boundaries to bio-production, especially in a large scale. Here, we foresee a clear advantage for the in situ integration (Figure 1A) in case high surface three-dimensional electrodes are used. Among these three-dimensional electrodes, gas diffusion electrodes (GDEs) seem most promising to us, due to their role in not only enhancing the CO2 mass transfer in aqueous media but also their ability to decrease the internal resistance by removing the bubbles covering the active surface areas of the electrodes when feeding CO2 directly in the aqueous media.9Song J.T. Song H. Kim B. Oh J. Towards higher rate electrochemical CO2 conversion: from liquid-phase to gas-phase systems.Catalysts. 2019; 9: 224https://doi.org/10.3390/catal9030224Crossref Scopus (58) Google Scholar In GDEs, CO2 feed is transported through the gas diffusion layer (Figure 2),9Song J.T. Song H. Kim B. Oh J. Towards higher rate electrochemical CO2 conversion: from liquid-phase to gas-phase systems.Catalysts. 2019; 9: 224https://doi.org/10.3390/catal9030224Crossref Scopus (58) Google Scholar allowing permanent availability of CO2 directly at the electrochemical reaction sites. The higher solubility of formate over CO2 in aqueous solution in turn assures the increased availability of feed for microbial synthesis. Further, the energetic efficiency of bioconversion using formate is higher compared to H2/CO2 (e.g., 80%–90% compared to 60%–80% in anaerobic acetogens).10Claassens N.J. Cotton C.A.R. Kopljar D. Bar-Even A. Making quantitative sense of electromicrobial production.Nat. Catal. 2019; 2: 437-447https://doi.org/10.1038/s41929-019-0272-0Crossref Scopus (79) Google Scholar In addition to formate, production of other C1 compounds such as methanol from CO2RR can be achieved. Methanol is more energy rich than formate and has been known as an established feedstock for microbial syntheses.10Claassens N.J. Cotton C.A.R. Kopljar D. Bar-Even A. Making quantitative sense of electromicrobial production.Nat. Catal. 2019; 2: 437-447https://doi.org/10.1038/s41929-019-0272-0Crossref Scopus (79) Google Scholar The selectivity of the products from CO2RR strongly depends on the electrode materials.11Li D. Zhang H. Xiang H. Rasul S. Fontmorin J.-M. Izadi P. Roldan A. Taylor R. Feng Y. Banerji L. et al.How to go beyond C1 products with electrochemical reduction of CO2.Sustainable Energy Fuels. 2021; 5: 5893-5914https://doi.org/10.1039/D1SE00861GCrossref Google Scholar For instance, while indium (In) or tin (Sn) (also Hg, Cd, etc.) are known for catalyzing CO2RR to formate, the oxidation state of copper (Cu2O) or addition of other metals to copper (e.g. Cu3Pt or Cu3Pd) can form methanol (although at different potentials). There are a number of external costs that need to be considered when developing processes for a bio-based and circular economy from lab bench to industrial reality. Product recovery through DSP, such as extraction, is required in any presented process design for turning CO2 and electric power to chemical products or fuels. It is of special importance for the designs with solution recirculation, due to the potentially toxic effect of bio-products (Figures 1A and 1B). For instance, high concentration of microbially produced carboxylic acids and their effect on the pH can have damaging effects on the cell membrane resulting in growth inhibition. Production of longer chain carbon products than C1 compounds such as terpenes, drugs, or even proteins not only increases the economic and energetic value but also makes the separation of the products more convenient. In addition to DSP, the quality of the gas feed is important particularly in the designs based on interfacing electrochemical and biological reactions (Figures 1A and 1B). Even when the electrochemical reactor is separated from the bioreactor (Figure 1C), impurities such as high percentage of oxygen can affect the CO2RR.4Hegner R. Rosa L.F. Harnisch F. Electrochemical CO2 reduction to formate at indium electrodes with high efficiency and selectivity in pH neutral electrolytes.Appl. Catal. B: Environ. 2018; 238: 546-556https://doi.org/10.1016/j.apcatb.2018.07.030Crossref Scopus (56) Google Scholar The flue gas from the cement industry, for instance, includes sulfur oxides and nitrogen dioxides in addition to dust and oxygen,12Vatopoulos K. Tzimas E. Assessment of CO2 capture technologies in cement manufacturing process.J. Clean. Prod. 2012; 32: 251-261https://doi.org/10.1016/j.jclepro.2012.03.013Crossref Scopus (99) Google Scholar which could disturb the electrochemical and microbial reactions and decrease the overall efficiency. In this case, an extra gas purification is required leading to increase in operational costs. CO2 purification and compression of flue gas through three different methods were calculated to require energy.12Vatopoulos K. Tzimas E. Assessment of CO2 capture technologies in cement manufacturing process.J. Clean. Prod. 2012; 32: 251-261https://doi.org/10.1016/j.jclepro.2012.03.013Crossref Scopus (99) Google Scholar As of today, ethanol and butanol produced by bio-based technologies are considered as potential alternatives to fossil-based transportation fuels. Syngas fermentation in an industrial scale is developed and pursued by some companies such as LanzaTech and its joint partner of Shougang group (Chinese Steel company), Genomatica, Kiverdi, IneosBio, and Coskata,13Liew F.E. Nogle R. Abdalla T. Rasor B.J. Canter C. Jensen R.O. Wang L. Strutz J. Chirania P. De Tissera S. et al.Carbon-negative production of acetone and isopropanol by gas fermentation at industrial pilot scale.Nat. Biotechnol. 2022; 40: 335-344https://doi.org/10.1038/s41587-021-01195-wCrossref PubMed Scopus (21) Google Scholar,14Sun X. Atiyeh H.K. Huhnke R.L. Tanner R.S. Syngas fermentation process development for production of biofuels and chemicals: a review.Bioresour. Technol. Rep. 2019; 7: 100279https://doi.org/10.1016/j.biteb.2019.100279Crossref Scopus (76) Google Scholar in particular for ethanol production (although IneosBio and Coskata stopped operation due to the operational and financial difficulties14Sun X. Atiyeh H.K. Huhnke R.L. Tanner R.S. Syngas fermentation process development for production of biofuels and chemicals: a review.Bioresour. Technol. Rep. 2019; 7: 100279https://doi.org/10.1016/j.biteb.2019.100279Crossref Scopus (76) Google Scholar). To make syngas fermentation even more economically and operationally feasible for the industry, remarkable efforts were taken, resulting in significant achievements over the past years. Different designs such as multi-stage fermentation or gas-liquid enhanced bioreactor for ethanol production have been patented.14Sun X. Atiyeh H.K. Huhnke R.L. Tanner R.S. Syngas fermentation process development for production of biofuels and chemicals: a review.Bioresour. Technol. Rep. 2019; 7: 100279https://doi.org/10.1016/j.biteb.2019.100279Crossref Scopus (76) Google Scholar Although the COVID-19 pandemic decreased the ethanol production in 2020, ethanol biorefineries are remaining major drivers in clean ethanol production in the US, Brazil, and certain parts in Asia and Europe.15RFA Ethanol Industry Outlook. Renewable Fuels Association, 2022https://ethanolrfa.org/file/2145/RFA%202022%20Outlook.pdfGoogle Scholar Despite the pandemic, 2.7 million tons of CO2 were captured in 2021 for ethanol biorefineries, which were used for further applications such as bottling and food processing. Production of other compounds than ethanol from syngas fermentation, such as acetate, isoprene or 3-hydroxypropionate, using genetically modified microorganisms were also patented.14Sun X. Atiyeh H.K. Huhnke R.L. Tanner R.S. Syngas fermentation process development for production of biofuels and chemicals: a review.Bioresour. Technol. Rep. 2019; 7: 100279https://doi.org/10.1016/j.biteb.2019.100279Crossref Scopus (76) Google Scholar Despite the growing progress observed in such biological syntheses, organic electrochemical syntheses on industrial scales seem not as mature. Thus far, electrochemical synthesis of valuable chemicals such as adiponitrile (a key intermediate for production of nylon-6,6) has been established for decades and used in industrial scales, for instance in Japan (Asahi Chemical in Nobeoka).16Botte G.G. Electrochemical manufacturing in the chemical industry.Electrochem. Soc. Interf. 2014; 23: 49-55https://doi.org/10.1149/2.f04143ifCrossref Scopus (0) Google Scholar Electrochemical organic synthesis has the advantages of high product selectivity and purity and simple integration with renewable energies as well as with biosynthesis due to the ambient temperature and pressure required for its operation, low number of reaction steps, and few polluting side products. However, its limited application in industry (especially without a known integration with developed biological synthesis in a large scale) can be seen as the consequence of several limits that have been in place up until now. These limits include missing suitable resources and manufacturing technologies; considerable excessive costs for capital expenditures, especially for implementing changes in existing production lines; lack of scientists and engineers being educated in integrating microbiology and electrochemistry; and lack of the collaboration between research and governmental sectors. To benefit from the electrochemical routes for the production of diverse, value-added, organic compounds from CO2 using renewable energies, strong partnerships between universities and research institutes, as well as in industry and government, are required. We are confident these partnerships in the long run will create value for society as well as shareholders. The authors acknowledge the support of the VIVALDI project that has received funding from the European Union’s Horizon 2020 research and innovation program under grant agreement 101000441 . This work was supported by the Helmholtz Association in the frame of the Integration Platform "Tapping nature’s potential for sustainable production and a healthy environment" at the UFZ . The idea of this article and the manuscript were conceived and written by P.I. and F.H. The authors declare no competing interests.