Microbial Electrosynthesis: Where Do We Go from Here?

Abstract

In the past decade, research in the field of microbial electrosynthesis (MES) has been driven forward by the development of cathode materials, electroactive bacteria or microbiome enrichment, and productivity improvements.As the close of three complete funding cycles for the field is reached, recent reviews have sought to refocus emphasis to the eventual application of MES; a means of measurably reducing CO2 waste via the formation of valuable products.Using present knowledge of bioelectrochemistry, and by learning lessons from adjacent fields, it becomes apparent that the simplest gains in performance are likely to come from advancements in the reactor rather than the biocatalysts. Varying the reactor and operating conditions of the system, however, require adapting these biocatalysts. The valorization of CO2 to valuable products via microbial electrosynthesis (MES) is a technology transcending the disciplines of microbiology, (electro)chemistry, and engineering, bringing opportunities and challenges. As the field looks to the future, further emphasis is expected to be placed on engineering efficient reactors for biocatalysts, to thrive and overcome factors which may be limiting performance. Meanwhile, ample opportunities exist to take the lessons learned in traditional and adjacent electrochemical fields to shortcut learning curves. As the technology transitions into the next decade, research into robust and adaptable biocatalysts will then be necessary as reactors shape into larger and more efficient configurations, as well as presenting more extreme temperature, salinity, and pressure conditions. The valorization of CO2 to valuable products via microbial electrosynthesis (MES) is a technology transcending the disciplines of microbiology, (electro)chemistry, and engineering, bringing opportunities and challenges. As the field looks to the future, further emphasis is expected to be placed on engineering efficient reactors for biocatalysts, to thrive and overcome factors which may be limiting performance. Meanwhile, ample opportunities exist to take the lessons learned in traditional and adjacent electrochemical fields to shortcut learning curves. As the technology transitions into the next decade, research into robust and adaptable biocatalysts will then be necessary as reactors shape into larger and more efficient configurations, as well as presenting more extreme temperature, salinity, and pressure conditions. The production of chemicals and fuels using CO2 and renewable energy as feedstocks is a key aspect in achieving a sustainable society [1.Sharon D.A.M. K.H.G.J. A Circular Economy in the Netherlands by 2050.Publisher Name: Government of the Netherlandshttps://www.government.nl/documents/policy-notes/2016/09/14/a-circular-economy-in-the-netherlands-by-2050Date: 2016Google Scholar]. As CO2 is the most oxidized form of carbon however, substantial energy is required to convert the inert molecule into a useful product. One of the research avenues being investigated for CO2 conversion is bioelectrochemistry (see Glossary), which allows for the production of more complex chemical compounds than purely electrochemical methods. The technology is rooted in the ability for microorganisms to take up electrons from solid-state electrodes, use them within their metabolism to convert CO2, and excrete a reduced chemical as an electron sink [2.Jourdin L. Strik D.P.B.T.B. Electrodes for cathodic microbial electrosynthesis processes: key-developments and criteria for effective research and implementation.in: Flexer V. Brun N. Functional Electrodes for Enzymatic and Microbial Bioelectrochemical Systems. World Scientific, 2017: 429-473Crossref Scopus (8) Google Scholar,3.Kerzenmacher S. Engineering of microbial electrodes.in: Harnisch F. Holtmann D. Bioelectrosynthesis. Springer International Publishing, 2019: 135-180Google Scholar]. This electricity-driven microbial conversion of CO2 is called microbial electrosynthesis (MES)[4.Rabaey K. Rozendal R.A. Microbial electrosynthesis — revisiting the electrical route for microbial production.Nat. Rev. Microbiol. 2010; 8: 706-716Crossref PubMed Scopus (1057) Google Scholar]. Figure 1 depicts the six main products formed in MES to date, alongside their current main industrial production methods (depicted in red). To date, 75% of all MES studies have reported solely acetate production, with a greater diversification of the product spectrum occurring only within the past few years [5.Flexer V. Jourdin L. Purposely designed hierarchical porous electrodes for high rate microbial electrosynthesis of acetate from carbon dioxide.Acc. Chem. Res. 2020; 53: 311-321Crossref PubMed Scopus (31) Google Scholar]. Over the past decade, since the original proof-of-concept [6.Nevin K.P. et al.Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds.mBio. 2010; 1: 1-4Crossref Scopus (627) Google Scholar], the focus of the MES research community has mainly been on developing cathode materials, enriching microbial catalysts and electroactive microorganisms, increasing productivity and selectivity, and shedding light on fundamental extracellular electron transfer (EET) mechanisms and microbial functions (with the relative research emphasis depicted visually in Figure 2A ). These steps have been vital to uncover further microorganisms and microbiomes, as well as demonstrating reasonable productivities. Together, these fundamental and applied advancements have continued to motivate the technology as a means of large-scale CO2 conversion. Looking forward to the next decade of MES, how will the field shift focus to accomplish the envisioned goal of replacing existing fossil-fuel production routes for these carbon-containing compounds? The following mainly focuses on biofilm-driven MES. Others have extensively discussed systems built around microorganisms in suspensions [7.Claassens N.J. et al.Making quantitative sense of electromicrobial production.Nat. Catal. 2019; 2: 437Crossref Scopus (79) Google Scholar]. In a recent article, Prévoteau and colleagues outlined in-depth the figures of merit envisioned to make MES a reality [8.Prévoteau A. et al.Microbial electrosynthesis from CO2: forever a promise?.Curr. Opin. Biotechnol. 2020; 62: 48-57Crossref PubMed Scopus (123) Google Scholar]. Further, Jourdin and coworkers recently provided a techno-economic analysis illustrating the combined cost and performance barriers to a profitable demonstration of MES [9.Jourdin L. et al.Techno-economic assessment of microbial electrosynthesis from CO2 and/or organics: An interdisciplinary roadmap towards future research and application.Appl. Energy. 2020; 279: 115775Crossref Scopus (25) Google Scholar]. Here, a different perspective is taken and the following question is asked: what are the barriers currently limiting MES, and how can this field shift its everyday research to overcome these limitations in the next ten years? Upon unpacking this question, it becomes apparent that many of the improvements in performance that are easily accessible are non-biological in nature, such as minimizing anode–cathode spacing and increasing salinity/temperature. These improvements have yet to be seriously considered as a way to improve the performance and commercial outlook of MES, which was the motivation for the writing of this opinion piece, providing a more in-depth perspective. Specifically, it needs to be considered that the vast majority of changes which can be made in reactor design, provide conditions that are unsuitable for current biocatalysts and cathode systems developed in the past decade. The remainder of this opinion will then discuss how the biocatalysts and reactors in MES systems will need to evolve, as there is a shift to more commercially-representative conditions. As the interaction between microbial catalysts and the electron-providing cathode is the central component of MES, discussing their relationship is essential as the field seeks to move to current and how can the of the and be to overcome limitations in and electron transfer To date, and microbial have been in MES et of chemicals by an microbial Microbiol. PubMed Scopus Google K.P. et of organic compounds from carbon dioxide is by a of Microbiol. PubMed Scopus Google Scholar], and a of electron transfer from the cathode to the have been or electron transfer [6.Nevin K.P. et al.Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds.mBio. 2010; 1: 1-4Crossref Scopus (627) Google K.P. et of organic compounds from carbon dioxide is by a of Microbiol. PubMed Scopus Google and electron transfer In CO2 to acetate conversion for has been to as electron the et of the route in electrosynthesis for microbial 8: Google and productivity of microbial electrosynthesis of Microbiol. 8: PubMed Scopus Google or was L. et production high microbial electrosynthesis of acetate from carbon Scopus Google Scholar]. In and production, mechanisms and microbial functions in complex be investigated further et al.Microbial electrosynthesis of from carbon and PubMed Scopus Google L. et carbon allows from CO2 up to high current Res. Scopus Google L. et to and acetate in from CO2: with CO2 rate and 2019; Scopus Google et and microbial PubMed Scopus Google et al.Microbial electrosynthesis of and from carbon Chem. Scopus Google et electricity-driven of and from CO2 with a microbial CO2 Scopus Google Scholar]. of the of electron it is that the cathode and be in close to to this and the of microbes be high to the rate of CO2 conversion. This of needs has many to the formation of a on the of the cathode [5.Flexer V. Jourdin L. Purposely designed hierarchical porous electrodes for high rate microbial electrosynthesis of acetate from carbon dioxide.Acc. Chem. Res. 2020; 53: 311-321Crossref PubMed Scopus (31) Google Scholar]. A and however, is to the eventual required current for MES discussed to be [8.Prévoteau A. et al.Microbial electrosynthesis from CO2: forever a promise?.Curr. Opin. Biotechnol. 2020; 62: 48-57Crossref PubMed Scopus (123) Google L. et al.Techno-economic assessment of microbial electrosynthesis from CO2 and/or organics: An interdisciplinary roadmap towards future research and application.Appl. Energy. 2020; 279: 115775Crossref Scopus (25) Google Scholar]. a as a and colleagues a of microbial with different and using [7.Claassens N.J. et al.Making quantitative sense of electromicrobial production.Nat. Catal. 2019; 2: 437Crossref Scopus (79) Google Scholar]. In this it was that with a high electron rate of a and a of bacteria of a current of only be in MES. an analysis the limitations of electron transfer of biocatalysts from the perspective of and the rate of microbial electron is then that the of the be means such as using or electrodes, which of MES studies have the from and coworkers to (see for can to what be required to current and the that may exist from this a carbon is taken as a which has been to an MES current of for an of L. et carbon allows from CO2 up to high current Res. Scopus Google Scholar]. such a can exist on the as well as on the of the carbon ). as and Figure the current from a purely for different and can be that with a a current from to can in be which is that in the to These that the is more than the are as the is of than the Figure the of the and of and electrodes, on the current with a which the to high current are microbial and it is that have been to be present the of such L. et carbon allows from CO2 up to high current Res. Scopus Google Scholar], the that factors than are limiting MES in these In research avenues in to and greater of MES One a more and focuses on in seeks to improve the from a purely electrochemical reactor factors such as and current The following the on these In methods to the on a and be a valuable for these and to there are limitations of the MES microorganisms, which their from the by and colleagues The the limitations of MES from a using the of the and as factors in limiting In as the of the and the of bacteria are are limitations reached, which the of reactor to One of the of operating MES is that ample CO2, and can be provided to all of microbes within the such that and of the of the can be An with on the of for is likely to into limitations of from the to the to the electrons electron from the may to the and product and in reduced or will productivity to ample is more complex for on the of is to only of the as is in systems of current MES studies as in Figure In the is to the porous current and have been reactors with [5.Flexer V. Jourdin L. Purposely designed hierarchical porous electrodes for high rate microbial electrosynthesis of acetate from carbon dioxide.Acc. Chem. Res. 2020; 53: 311-321Crossref PubMed Scopus (31) Google Scholar]. MES research to has placed substantial emphasis on reactor to improve L. et carbon allows from CO2 up to high current Res. Scopus Google F. et from to a 2019; Scopus Google et microbial electrosynthesis reactor Microbiol. PubMed Scopus Google et electrodes for effective and of carbon dioxide to microbial Scopus Google Scholar], to the reactor can for A in is the between the and As discussed by Prévoteau and the within the will a of the operating [8.Prévoteau A. et al.Microbial electrosynthesis from CO2: forever a promise?.Curr. Opin. Biotechnol. 2020; 62: 48-57Crossref PubMed Scopus (123) Google Scholar]. the of the and cathode to will then have the electrochemical as the will be the A of electrodes, is in the which in reduced and current on the of the A analysis of the and 2019; Scopus Google of high electrodes are an the need for a is by an reactor design, that a be As a Figure (see the how the current for different only the rate is the a motivation for greater and in MES reactors can be which can then be using to of MES all from to has been and is necessary to of the and for and To only and the of operating S. et the of operating in microbial electrosynthesis: a Chem. Chem. 2019; PubMed Google Scholar], and current and on et in a microbial to acetate from CO2 and Chem. Chem. PubMed Google Scholar], and coworkers from their reactor F. et from to a 2019; Scopus Google Scholar]. and colleagues recently the between and and F. et on the of electromicrobial 2020; Scopus Google Scholar]. only a was that as the its and its in to a following their a or to the and may the of high energy a reasonable reactor a commercial with and [2.Jourdin L. Strik D.P.B.T.B. Electrodes for cathodic microbial electrosynthesis processes: key-developments and criteria for effective research and implementation.in: Flexer V. Brun N. Functional Electrodes for Enzymatic and Microbial Bioelectrochemical Systems. World Scientific, 2017: 429-473Crossref Scopus (8) Google V. Jourdin L. Purposely designed hierarchical porous electrodes for high rate microbial electrosynthesis of acetate from carbon dioxide.Acc. Chem. Res. 2020; 53: 311-321Crossref PubMed Scopus (31) Google K. et electrodes for microbial Opin. Biotechnol. PubMed Scopus Google can be as a methods be such for that the discussed be that energy be replacing the water to date, the focus of microbial electrosynthesis (MES) development has been on the with water the for have been made to the with a et acetate production from carbon dioxide using a microbial electrosynthesis with PubMed Scopus Google Scholar], is required to make this and [9.Jourdin L. et al.Techno-economic assessment of microbial electrosynthesis from CO2 and/or organics: An interdisciplinary roadmap towards future research and application.Appl. Energy. 2020; 279: 115775Crossref Scopus (25) Google Scholar]. that and production are a decade of it is to MES with a more and of the only the main cost of MES, to of the substantial [9.Jourdin L. et al.Techno-economic assessment of microbial electrosynthesis from CO2 and/or organics: An interdisciplinary roadmap towards future research and application.Appl. Energy. 2020; 279: 115775Crossref Scopus (25) Google Scholar]. As adjacent research fields have recently up the development of catalysts for the of these advancements can be into MES systems in the future S. et of CO2 and as a to carbon chemicals with to electricity Energy. 2019; Scopus Google Scholar]. a of for the of and with the energy of the and the different can be made from replacing water or than water the organic high which is in to the current in MES are in of or to a a means of the an provide the to make a valuable product. This however, is it needs to be that the of the product well with the cathode product in of production and Further, the goal of MES is to substantial of waste CO2, then the product be and techno-economic then the of the water will to to its of for is can be and current are to with the As the field the of replacing the as a development for MES of and for the Microbial of CO2 to to or and 1 cathode cathode in a To date, the focus of microbial electrosynthesis (MES) development has been on the with water the for have been made to the with a et acetate production from carbon dioxide using a microbial electrosynthesis with PubMed Scopus Google Scholar], is required to make this and [9.Jourdin L. et al.Techno-economic assessment of microbial electrosynthesis from CO2 and/or organics: An interdisciplinary roadmap towards future research and application.Appl. Energy. 2020; 279: 115775Crossref Scopus (25) Google Scholar]. that and production are a decade of it is to MES with a more and The of the only the main cost of MES, to of the substantial [9.Jourdin L. et al.Techno-economic assessment of microbial electrosynthesis from CO2 and/or organics: An interdisciplinary roadmap towards future research and application.Appl. Energy. 2020; 279: 115775Crossref Scopus (25) Google Scholar]. As adjacent research fields have recently up the development of catalysts for the of these advancements can be into MES systems in the future S. et of CO2 and as a to carbon chemicals with to electricity Energy. 2019; Scopus Google Scholar]. a of for the of and with the energy of the and the different conditions. can be made from replacing water or than water the organic high which is in to the current in MES are in of or to a a means of the an provide the to make a valuable product. This however, is it needs to be that the of the product well with the cathode product in of production and Further, the goal of MES is to substantial of waste CO2, then the product be and techno-economic then the of the water will to to its of for is can be and current are to with the As the field the of replacing the as a development for MES of and for the Microbial of CO2 to to or and 1 cathode cathode in a In and will the of an MES system, providing a for different These are from many of the fundamental in the field are required more and more as microbial productivity to In MES a of different operating conditions have been such as the of L. et microbial electrosynthesis to and operating PubMed Scopus Google et of on and acetate production by an PubMed Scopus Google Scholar], applied cathode et of applied and carbon on acetate production microbial CO2 Scopus Google Scholar], applied current et to Scopus Google Scholar], or of L. et carbon allows from CO2 up to high current Res. Scopus Google et electricity-driven of and from CO2 with a microbial CO2 Scopus Google Scholar]. The of feeding CO2 as or as S. et of reactor for carbon dioxide into organic PubMed Scopus Google et al.Microbial electrosynthesis high with 2020; PubMed Scopus Google Scholar], and of have been et al.Microbial electrosynthesis (MES) from CO2 is to in renewable energy Scopus Google Scholar]. it is expected that the of the temperature, salinity, and may to substantial gains in the of MES systems ). discuss how increasing of these can be to be and how to current microbes are to these water and for as these with substantial is which the up to in a in electrochemical of catalysts an and a in of which the for is to by factors from to as in Figure and for in Figure (see the The for MES in of however, is that formation in MES has only been in with to microbial be to however, then be purely by a in in the is as by microbial operating conditions with microbial transfer and of et production and microbial community in and microbial 2019; PubMed Scopus Google et for microorganisms in microbial electrochemical Microbiol. Rev. PubMed Scopus Google of by a 2: Scopus Google et and of the PubMed Scopus Google et microorganisms in Rev. Microbiol. 2019; PubMed Scopus Google Scholar]. and colleagues the community from a that only for the conversion of CO2 to et an community to an production a as cathodic 2020; PubMed Scopus Google Scholar]. and up to N. K. of from CO2 by microbial electrosynthesis (MES) high Chem. Biotechnol. Scopus Google Scholar]. In to the of the the can be made more the and the in the This is only necessary from a perspective [8.Prévoteau A. et al.Microbial electrosynthesis from CO2: forever a promise?.Curr. Opin. Biotechnol. 2020; 62: 48-57Crossref PubMed Scopus (123) Google Scholar], a high the current and in electrodes by the The of operating is the need to or MES microbial that can it [8.Prévoteau A. et al.Microbial electrosynthesis from CO2: forever a promise?.Curr. Opin. Biotechnol. 2020; 62: 48-57Crossref PubMed Scopus (123) Google Scholar]. are as and extreme et for microorganisms in microbial electrochemical Microbiol. Rev. PubMed Scopus Google of Scholar]. main can be towards of microorganisms for MES such as applied in et of a from a Microbiol. PubMed Scopus Google or of microorganisms from extreme or et for microorganisms in microbial electrochemical Microbiol. Rev. PubMed Scopus Google et and efficient electrochemical of and in high PubMed Scopus Google et of the electrochemical of with the and microbial of the 1: Scopus Google or engineering [8.Prévoteau A. et al.Microbial electrosynthesis from CO2: forever a promise?.Curr. Opin. Biotechnol. 2020; 62: 48-57Crossref PubMed Scopus (123) Google et microorganisms in Rev. Microbiol. 2019; PubMed Scopus Google Scholar]. As an may as for via et formation by is by and PubMed Scopus Google Scholar]. and colleagues recently a from a et of and the of microbial electrosynthesis with Microbiol. 2019; PubMed Scopus Google Scholar]. was of reducing CO2 to acetate current on the and and the of the microbial increasing the can for the to within the of the The the the the of with The which can be to improve performance is the which can be to CO2 it is how the and of MES are by CO2 which CO2 the rate and rate are the of electrodes and current is expected to be a greater on CO2 in the Further, operating and have a on CO2 as for in Figure A is to the CO2 as has been in catalysts et CO2 recent and current Chem. Scopus Google Scholar]. In microorganisms are such as in et high pressure and in a reactor PubMed Scopus Google Scholar]. of increasing CO2 pressure reactor to CO2 transfer to the biocatalysts that are and be the use of electrodes S. et of in microbial electrosynthesis from carbon Res. PubMed Scopus Google Scholar], reactors F. et from to a 2019; Scopus Google Scholar], and et electrodes for effective and of carbon dioxide to microbial Scopus Google K.P. et and cathode for waste to valuable using microbial electrochemical PubMed Scopus Google Scholar], investigated to improve CO2 to the biocatalysts, for acetate or was that increasing the CO2 rate pressure and electron and carbon towards and via transfer of CO2 L. et to and acetate in from CO2: with CO2 rate and 2019; Scopus Google Scholar]. are an route forward for MES, a of the salinity, temperature, and is likely to a key in demonstration and up of high rate to of will be as in nature, the the and the temperature, the more the to thrive as with bacteria et for microorganisms in microbial electrochemical Microbiol. Rev. PubMed Scopus Google Scholar]. a way to the may be to the in the This was for application using for electricity production et for microorganisms in microbial electrochemical Microbiol. Rev. PubMed Scopus Google Scholar]. for MES using a and this may the is and high may for high current and/or in which the is likely to shift from the exist between MES and electrochemical on of the are more or are water and and lessons from reactor design, and as well as and design, and be taken from of and be to MES A analysis of the and 2019; Scopus Google S. S. catalysts for carbon dioxide conversion into 2019; Google Scholar]. all of these it is opinion that a technology needs to be developed to improve the commercial of MES and all rate and limiting from microorganisms to reactor is (see and will require from a of such as microbiology, (electro)chemistry, engineering, and that the non-biological are more easily (with the of and reactor and is the that can be made the to improve MES productivity and The changes required will likely in on the microorganisms in the In the future, the of and microorganisms will and for to and and/or to the production of a of products from CO2 by MES. The engineering of microorganisms for MES the have than In the MES be technology for the production of and/or to further by adapting current to or enriching microbial catalysts from extreme or In to biofilm-driven MES as discussed systems on microorganisms in further are within the electrochemical reactor or within a to an electrochemical reactor that an electron and/or carbon or for microbial in reactor and will provide the for and is limiting a current in the of and a and be built and as a for MES and as a for be in the or from and/or to high MES reactor design, what can come from large-scale reactors and large-scale electrochemical MES be by or by water the for MES is limiting a current in the of and a and be built and as a for MES and as a for be in the or from and/or to high MES reactor design, what can come from large-scale reactors and large-scale electrochemical MES be by or by water the for MES This is by and a from for and of the of and in the of the colleagues of the of for the valuable on the with use of microorganisms in the cathode of a system, that are of up electrons or from the that the use of microorganisms and/or in electrochemical to to or electrons from an or of microorganisms that to and to a an the of current of a or microorganisms to electrons with an electrons to an or electrons from a mechanisms by which microorganisms electrons with an extracellular electron occurring compounds and electrodes, the microorganisms that in that are to most of microorganisms that in high electricity-driven in which microorganisms take up electrons from the cathode and carbon such as microorganisms in a in a that to the of the of electrons the materials, and the of in and

Topics & Concepts