Journal Archive

Johnson Matthey Technol. Rev., 2022, 66, (4), 455
doi: 10.1595/205651322X16621070592195

Enhancing Microbial Electron Transfer Through Synthetic Biology and Biohybrid Approaches: Part II

Combining approaches for clean energy


  • Benjamin Myers
  • Bioelectronics Laboratory, Regenerative Medicine and Cellular Therapies Division, School of Pharmacy, Biodiscovery Institute, University of Nottingham, University Park, Clifton Boulevard, Nottingham, NG7 2RD, UK
  • Phil Hill
  • School of Biosciences, University of Nottingham, Sutton Bonington Campus, Sutton Bonington, Leicestershire, LE12 5RD, UK
  • Frankie Rawson
  • Bioelectronics Laboratory, Regenerative Medicine and Cellular Therapies Division, School of Pharmacy, Biodiscovery Institute, University of Nottingham, University Park, Clifton Boulevard, Nottingham, NG7 2RD, UK
  • Katalin Kovács
  • School of Pharmacy, Boots Science Building, University of Nottingham, University Park, Clifton Boulevard, Nottingham, NG7 2RD, UK
  • Email: *Frankie.rawson@nottingham.ac.uk; **Katalin.kovacs@nottingham.ac.uk

PEER REVIEWED

Received 7th February 2022; Revised 7th June 2022; Accepted 10th June 2022; Online 10th June 2022


Article Synopsis

It is imperative to develop novel processes that rely on cheap, sustainable and abundant resources whilst providing carbon circularity. Microbial electrochemical technologies (MET) offer unique opportunities to facilitate the conversion of chemicals to electrical energy or vice versa by harnessing the metabolic processes of bacteria to valorise a range of waste products including greenhouse gases (GHGs). Part I (1) introduced the EET pathways, their limitations and applications. Here in Part II, we outline the strategies researchers have used to modulate microbial electron transfer, through synthetic biology and biohybrid approaches and present the conclusions and future directions.

 

Engineering Biology Approaches for Extracellular Electron Transfer Modulation

Increasing the conductivity of pilin-based bacterial nanowires via aromatic amino acid content modification of protein monomer sequences has been an interesting target for the modulation of extracellular electron transfer (EET) mechanisms. Tan and colleagues (2) found that replacing the tyrosine and phenylalanine residues at the carboxyl terminus of the Geobacter sulfurreducens PilA monomer with tryptophan yielded a strain expressing pili with conductivities over 500-fold greater than G. sulfurreducens wild-type. In another study (3), the authors found that expression of the aromatic-amino acid rich, highly conductive Geobacter metallireducens PilA monomer in G. sulfurreducens produced currents over 5000-fold greater than G. sulfurreducens wild-type. These findings strengthen the correlation between aromatic amino acid content and pili conductivity, offering opportunities to improve pili conductivity via amino acid sequence modification of the pilus monomer.

The presence of the T4aP assembly systems in many other bacterial species offers a great opportunity to confer EET abilities to non- or poorly conductive organisms. Pseudomonas aeruginosa has been subjected to two different biological engineering approaches by Liu and colleagues (4) to enhance the EET ability of this organism by heterologous expression of G. sulfurreducens PilA, alongside the modification of its native PilA with the elements of G. sulfurreducens PilA thought to impart conductivity. These modifications included the truncation at the C-terminus to 61 amino acids in length (from 143) and increasing aromatic amino acid content, producing the strains P. aeruginosa GsPilA and PaPilA (5). The recombinant pili of both strains could interact with the native assembly machinery, forming pili complexes with increased charge transfer than wild-type P. aeruginosa. P. aeruginosa GsPilA displayed conductivity comparable to G. sulfurreducens PilA, and P. aeruginosa PaPilA was 140 times more conductive than native PilA. Remarkably, the modified P. aeruginosa PaPilA displayed conductivity with a seven-fold increase over the G. sulfurreducens PilA. This suggests modifying the monomer sequence of other T4aP-producing organisms may improve native EET capabilities.

In another study, heterologous expression of the G. sulfurreducens PilA in the model organism Escherichia coli enabled conductive nanowire expression under aerobic conditions (6). The use of E. coli enables the leverage of a much greater genetic toolkit, including the possibility of synthetic amino acid inclusion into the monomer sequence to confer additional functionality. This was achieved by expressing the native T4aP from enterohemorrhagic E. coli in a non-pathogenic strain while replacing the native PpdD pilin gene for G. sulfurreducens PilA conductive pili monomer producing the strain E. coli GPN (6, 7). While the recombinant pili were shown to have similar conductivity to G. sulfurreducens PilA ex vivo , it is unclear whether the recombinant strain E. coli GPN can utilise the EET mechanism to achieve the same levels of EET as the wild type in microbial electrochemical technologies (MET) applications. Conducting microbial fuel cells (MFCs) studies using the E. coli GPN chassis would be a vital continuation of this research to assess the capabilities of recombinant nanowire exoelectrogenic potential in vivo . Furthermore, researchers have recently designed a conductive type-1 pilus from E. coli , using synthetic amino acids to increase electron transfer potential, alongside conjugation with gold nanoparticles to further boost filament conductivity (8), producing an organic biohybrid conductive nanowire. PilA sequence modification also provides opportunities to add peptide tags to conductive nanowires, allowing novel environmental sensing applications and increasing affinity to other molecules (6, 9).

To date, several research groups have successfully expressed the Shewanella onedesis MTR-1 direct EET pathway in E. coli (1012). First achieved in 2010, Jensena et al . demonstrated that expression of MtrCAB could allow electrochemical connections (or ‘wiring up’ (13)) between bacteria incapable of metal reduction and the solid mineral α-Fe2O3. Specifically, in E. coli expression of MtrCAB allowed the reduction of insoluble Fe(III) four times faster than the wild type strain, demonstrating that MtrCAB recombination is a potential route to produce synthetic exoelectrogenic bacterial chassis.

Other studies have demonstrated that MtrCAB expression can shift the metabolism of engineered E. coli strains towards reduced products (14). Researchers in 2020 achieved 90% increases in succinate production (from fumarate) via an E. coli strain engineered with the MtrCAB membrane proteins from S. onedesis, using the soluble mediator neutral red as an intermediate (14). Furthermore, the study’s authors achieved a shift towards reduced fermentation products in a microbial electrosynthesis systems (MES) bioreactor using glucose as a carbon source. With electrical stimulation of 69.6 ± 5.5°C charges to the anode, an engineered E. coli T110 strain expressing the MtrCAB complex produced 64.7% more succinate and 34.1% less acetate than a control non-electroactive E. coli T110 strain (14) indicating an increased rate of electron assimilation and utilisation. While these studies demonstrate that S. onesesis EET pathways can be used to produce microbial chassis capable of reducing oxidised carbon sources to valuable chemicals and fuels, the technology is not yet at a state where the EET rate of recombinant strains can be increased over that of the native exoelectrogenic bacteria. Furthermore, S. onedesis is capable of direct ET (although short-range) however this ability has not yet been achieved in engineered E. coli strains by MtrCAB expression alone. This point highlights the complexity of native EET mechanisms and indicates the expression of EET pathways may be under some form of post-translational control. Recent advancements have achieved both anodic (15) and cathodic (16) EET in E. coli strains expressing the Mtr1 pathway, by modifying the ccm genes regulating cytochrome maturation. These findings suggest that simply expressing the Mtr pathway alone is not sufficient to enable direct EET, control of protein synthesis and maturation is required to express Mtr1 cytochromes in the correct ratios and locate to the required intracellular positions to enable increased electron flux (17).

An interesting development in the engineering and design of recombinant electroactive bacteria (EAB) is the finding that redox-active shuttle molecules can interact directly with genetic regulation systems (1821). A 2017 study demonstrated that the redox-active, membrane-permeable electron shuttle molecule pyocyanin could be used to intracellularly activate the SoxRS regulon in E. coli , stimulating the expression of a range of genes under its control (18) via modifying the voltage applied to an electrode. This work offers broad opportunities in controlling gene expression via electrical stimulation, of particular interest to MES reactions where modulating the production of a range of valuable reduced chemical commodities is a longstanding goal (22).

Biohybrid Approaches for Extracellular Electron Transfer Modulation

An alternative approach to bridge the gap between cellular redox machinery and MET circuitry can be achieved via the use of conductive nanomaterials, which have been extensively reviewed (2329). Advancements in nanoscale material engineering and synthesis have enabled the possibility of replicating biological EET mechanisms with conductive nanoscale structured materials. Properties such as high conductivity, large specific surface areas and biocompatibility make conductive nanomaterials highly attractive to enhance the EET rate of EAB, by bridging the gap between the microbial redox machinery and electrodes (27, 29, 30) as seen summarised in Figure 1 and described in more detail below.

Fig. 1.

Locations of nanomaterial modification to increase bacterial EET: (a) inside-membrane, with nanomaterials bridging the gap between intracellular microbial redox machinery and electrode; (b) cell-electrode interface, where highly structured nanomaterials increase electrode surface area and offer increased sites for biofilm attachment; (c) biofilm modification, providing a conductive scaffold throughout the biofilm via the addition of conductive nanomaterials or redox-active particles to extend the spatial range of EET; and (d) interspecies modifications, where nanomaterials provide an electron transfer conduit between a mixed microbial culture. Reprinted from (31), Copyright (2018), with permission from Elsevier

Nanoscale materials, such as carbon nanotubes (CNT), graphene oxide (GO), metal nanoparticles and a range of synthetic conductive polymers have been employed based on their remarkable conductive properties and nanometre size, enabling electrochemical interactions with cellular systems (32). Termed ‘biohybrid’ systems, nanomaterial-based EET technologies have been employed to form a connection between microbial redox centres and electrodes of MET at several locations: inside-membrane; at the interface; inside biofilm; and interspecies (29).

Biohybrid Modifications by Location

Inside-membrane modifications (Figure 1(a)) are those where nanomaterials probe the cellular interior and bridge the gap between internal redox machinery and electrode (31). Cell-electrode interface modifications (Figure 1(b)) rely on highly structured nanomaterials to increase electrode surface areas and redox site availability or to provide a framework for increased biofilm attachment (28, 29). Inside-biofilm modifications (Figure 1(c)) use nanomaterials to provide a conductive scaffold throughout a biofilm, increasing the spatial range of EET (33). Nanomaterials were also employed to provide an electron transfer conduit between a multispecies microbial community (34) (Figure 1(d)); however, these modifications are outside the remit of this review.

Inside-Membrane Modifications

Early studies focused on fabrication of electrodes from single walled CNT (SWCNTs) functionalised with an osmium(II) bipyridine complex (Osbpy). These were successfully used to convert biologically generated currents from Proteus vulgaris and will be discussed below. While focused on eukaryotic cells, researchers have devised strategies enabling electrochemical communication with the cellular interior. CNTs are particularly suited to this application, as their high aspect ratio enables penetration of membranes to access the cellular interior without affecting viability. A 2012 study successfully interfaced DNA-wrapped CNTs with the RAW 264.7 mouse macrophage cell line (35). DNA-functionalised CNTs were deposited on an indium-tin-oxide glass chip in a vertical alignment, forming a ‘nanoelectrode array’ capable of self-insertion in the membrane and detecting the reduction of the methylene blue redox probe after electrochemical stimulation. These findings demonstrate that CNTs can span biological membranes to access the intracellular environment without causing cell death, alongside the potential to modify CNTs with biomolecules to confer additional functionality. Building on this approach, multiple studies have demonstrated that CNT-cell interfacing could also be achieved via centrifugation, eliminating the need to modify the CNT nanoelectrode with DNA (3638). Applying similar methodologies to poor EAB may offer potential in enabling EET abilities. However, differences in prokaryotic and eukaryotic cell wall physiology are a barrier. While eukaryotic cells have single-layer membranes, allowing relatively straightforward CNT insertion, bacterial cell membranes, especially the Gram-negative family in which many of the EAB reside, have multi-layered protective membranes (39). A nanoelectrode array would need to be of sufficient length to penetrate the bacterial envelope to connect with internal redox centres, with no loss of conductivity or increases in resistance or toxicity. Furthermore, the increased centrifugal forces required to penetrate thicker bacterial envelopes may reduce viability.

An alternative membrane insertion methodology involves functionalising CNTs with species-specific lipids, allowing natural compatibility and insertion within phospholipid membranes (4042). These synthetic ‘CNT-porins’ replicate biological membrane channels and with lumen diameters of approximately 1 nm have been demonstrated to facilitate transport of biomolecules to the cellular interior (41, 43). Furthermore, as their length is determined by a sonication step (44) it may be possible to produce CNT-porins of a length sufficient to penetrate the bacterial envelope. CNT-porins have been successfully used as a synthetic drug membrane conduit in eukaryotic cells (43) and may offer a novel route to allow EET in microbial species without efficient native EET mechanisms. However, materials such as CNTs can have antimicrobial properties (45), causing loss of membrane function and structure (46). Any system complexing CNTs with bacterial membranes must be carefully designed to not affect the cell membrane viability.

At-Interface Modifications

All MET include an electrode acting as the electron acceptor or donor. MFCs were the first form of MET to be developed, largely designed with carbon-based electrodes such as glassy carbon, graphite, carbon paper and carbon cloth (32). Early designs used the addition of exogenous electron mediators to shuttle the charge between the cell and electrode. However, the mediator compounds required constant replenishment, adding cost, complexity and environmental issues surrounding their disposal (47). The discovery of direct EET methods removed some of this complexity, leading to an increase of charge and power densities produced. However, the overall charge transfer efficiency of direct EET mechanisms is fundamentally limited by the number of cells in physical contact with the electrode (48, 49). G. sulfurreducens nanowires are an example of a naturally-evolved strategy to increase the biofilm loading capacity of an electron donor or acceptor (50). In a synthetic approach to the same goal, three-dimensional (3D) conductive nanomaterial-functionalised electrodes have been extensively studied (5155). By decorating electrode surfaces with highly structured nanomaterials, specific surface areas are vastly increased providing more locations for biofilm attachment and EET to occur in an example of ‘at interface’ biohybrid MES.

CNTs and GO, are some of the most well-studied nanomaterials in MET applications, having shown successes in enabling increased microbial EET rates through a combination of increased surface areas and high conductivity. Peng et al . found that S. onedesis MTR-1 current generation in an electrochemical cell was increased 82-fold with a CNT-modified electrode, from 0.117 μA cm–2 to 9.70 μA cm–2. The study’s authors theorised that heterogenous Mtr cytochromes exhibit a ‘sluggish’ form of electron transfer, and the favourable electron kinetics of CNTs, rather than increase of electrode surface area solely, contributed to the increase in current generation (56). In contrast, Zhao and colleagues designed a highly structured nanoelectrode ‘net’ from GO and CNTs, vastly increasing the electrode surface area and number of cells in direct contact. This resulted in a 60-fold increase in current density generation (from 20 μA cm–2 to 120 μA cm–2), as compared to a naturally grown anodic biofilm (57). Similarly, a research group achieved 25-fold increases in anodic, and 74-fold increases in cathodic current density over that of the naturally occurring biofilms via the use of a GO mesh electrode with embedded S. onedesis MTR-1 biofilm (58).

Coating electrode surfaces in conductive polymers, such as osmium redox polymers have also been employed to increase bacterial EET rates, by improving biocompatibility and biofilm adhesion (5961) and allowing direct EET, in organisms previously considered incapable of this form of electron transfer (62, 63). For future nanostructured electrode design, looking outside of the CNT-GO paradigm, it may be beneficial to take advantage of the additional properties and functionalities offered by alternative materials.

Inside-Biofilm Modification

Tuning the conductivity of biofilms via the addition of conductive nanoparticles is an alternative strategy to increase the rate of bacterial EET. Not all EAB can generate an extracellular conductive matrix, and research suggests thick biofilm growth can suppress EET in strains incapable of long-range DET (64). Furthermore, while native G. sulfurreducens nanowires are highly conductive (65), there is still potential for further improvement. Another approach to increase the spatial range of EET in EAB is to ‘dope’ the system with conductive particles, generating a ‘biohybrid’ synthetic extracellular conductive matrix, or strengthening an existing one. A range of metal and carbon-based materials have been studied (33, 6669). Zhang and colleagues (33) designed a hybrid system, wiring naturally occurring anodic biofilms with a conductive scaffold of CNTs, forming ‘synthetic nanowires’ of the same principle as G. sulfurreducens conductive filaments. This system displayed 40% increases in current generation over a naturally formed biofilm, with 53% decrease in start-up time before current generation occurred. Chen et al . (70) developed a similar system incorporating gold nanoparticles into G. sulfurreducens biofilms, reducing charge transfer resistance of the native biofilm and achieving anodic current density increase of 40% over the native biofilm, indicating the potential of this strategy.

An advantage of biohybrid-biofilm modification is the relative simplicity of material integration compared to strategies involving synthetic biology or nanoparticle incorporation within bacterial membranes; the systems involve either simple addition of nanoparticles to an anodic MFC chamber (70) or an absorption and filtration process (33). In addition, the antimicrobial potential of puncturing bacterial membranes with CNTs is eliminated as biofilm modifications are applied extracellularly. Furthermore, Kato et al . (68) found that doping MFC biofilms with iron-oxide minerals increased the charge densities produced by Geobacter spp without conductive nanowire expression systems, while reducing current density in the nanowire-producing G. sulfurreducens, indicating that iron-oxide-mineral addition produced a microbe-mineral network, rather than a conductive mineral-doped biofilm. The study’s authors argued this microbe-mineral network is metabolically favourable as an EET pathway, due to the large energy expenditure of nanowire expression and that expressing conductive filaments is the EET pathway of last resort for G. sulfurreducens (68). Comparing current densities produced via doping the biofilm of a EAB strain with conductive particles with a naturally formed biofilm would be a promising experiment to test this hypothesis, potentially allowing a straightforward method to tune biofilm conductivity. However, as this strategy is based on extending the spatial range of EET; it must employ a bacterium capable of high-rate EET, rather than conferring exoelectrogenic abilities to a non- or poorly electroactive organism.

Additional Extracellular Electron Transfer Modulation Strategies

Redox-active and conductive polymers have also been applied as ET conduits at the microbe-electrode interface (7173). While bacteria outlined previously have the capability of directly connecting with electrodes, many organisms cannot. Thus, large classes of microbial species require indirect, ‘mediator’ based systems to perform EET. ‘Mediator based’ EET is classified as an indirect mechanism, as the shuttle compounds are solubilised and charge transported throughout the liquid media. However, a novel approach is blurring the classifications of EET by immobilising redox mediator compounds onto electrode surfaces (7476). By creating synthetic or ‘biohybrid’ redox centres on the electrodes of MET, exoelectrogenic microbial EET can be ‘boosted’ and allow EET capabilities in organisms traditionally considered as ‘non-exoelectrogenic’. Immobilised mediator compounds differ in their mechanism of electron transfer; redox active materials contain residues that are oxidised and reduced in cyclical manners, accepting and donating electrons between the microbial catalyst and electrode and acting as intermediate electron ‘batteries’ or ‘capacitors’. In contrast, conductive polymers act as ‘wiring’, transporting electrons through a conductive inner core formed by the stacking of pi:pi orbitals within the internal structure. Conductive polymers are generally capable of higher ET rates, although redox active polymers can be tuned to a greater degree. As ET occurs on redox-active residues located on sidechains of the polymer structure, the potential to modify redox active polymers is greater than the inner-core located residues of conductive polymers. While both can be applied to boost the EET capabilities of MET, the properties must be matched to the desired application. For example, conductive polymers display optimum ET rates in acidic conditions, while redox-active polymers can be manipulated for a pH optimum of choice. Two example families of redox-active and conductive polymers are based on osmium, and quinone respectively.

Osmium-based polymers (OBP) have shown success in enabling direct EET in otherwise incapable organisms, through the decoration of electrode surfaces and electrons travelling via electron hopping along redox-active osmium units within the polymer structure. Both prokaryotic and eukaryotic osmium-facilitated EET has been observed, including both Gram-negative dual membraned (~15 nm) and Gram-positive single membrane (~35 nm) cell envelopes (75) suggesting OBP enabled the exchange of electrons from the cell surface, rather than penetrating the cell to access intracellular redox centres. Indeed, the observation that direct EET was possible through the thick peptidoglycan cell wall of Gram-positive bacteria through OBP-electrode functionalisation suggested an electrochemical interaction between surface-bound cell wall components and OBP facilitated EET. To demonstrate this effect, Pankratova et al . coated gold disk electrodes with an osmium redox polymer (Os(2,2′-bipyridine)2-poly(N -vinylimidazole) 10Cl]2+/+) and tested the electrochemical response in the presence and absence of Gram-positive Enterococcus faecalis cells. While no current generation was observed in the absence of cells or osmium polymer, the inclusion of bacterial cells led to a current response of 18 ± 1 μA cm–2. Considering the thick peptidoglycan cell wall of E. faecalis, it is unlikely that the osmium polymer directly communicated with internal redox centres indicating the ability of osmium polymers to mediate electron flow across cellular envelopes (73). The fact that E. faecalis , and other Enterococci are frequently found as part of the natural microbial consortia of MFC inocula complicate the situation, indicating another member of the consortium may produce a mediator compound that can be utilised by Enterococci to facilitate EET. In eukaryotic yeast cells, researchers observed electrochemical interactions between cells and electrodes modified with an osmium bipyridine polymer. Again, the surface topography of the modified electrode, with peaks smaller than the cell wall indicated ET did not occur as a result of membrane penetration. However, control experiments removing the OBP led to no electrochemical peak upon cyclic voltammetry scanning, indicating the OBP was facilitating charge transfer from the cellular exterior. While these findings challenge previous assertions about cell wall conductivity and electron transfer, the authors could not explain the phenomenon. Current understandings of cell wall physiology may need to be re-evaluated to gain a deeper understanding of the travel of electrons through the cell walls of eukaryotic microorganisms (77).

The use of more than one functional nanomaterial in combination can overcome the shortcomings of any individual material (7880). For example, GO is a highly conductive, one-dimensional carbon network capable of forming 3D structures with high specific surface areas, however these are prone to cross-linkage and aggregation. Modification with multi-walled CNTs (MWCNTs) can provide a supportive scaffold, reducing agglomeration between graphene sheets and producing a macroporous electrode surface for increased bacterial adherence. To demonstrate this system, Zou et al . (81) constructed a S. putrefaciens -inoculated MFC using a hybrid MWCNT-reduced GO (rGO) anode. The system achieved current density outputs of 44%, 22% and 182% increase over MWCNT, rGO and bare carbon cloth anodes respectively (rGO:MWCNT = 2.09 ± 0.05 A m–2; MWCNT = 1.45 ± 0.04 A m–2; rGO = 1.71 ± 0.05 A m–2; bare carbon cloth = 0.74 ± 0.01 A m–2). In addition, the rGO:MWCNT anode achieved power density increases of 86% and 57% over MWCNT and rGO anodes respectively (rGO:MWCNT = 789 mW m–2; MWCNT = 423 mW m–2; rGO = 500 mW m–2) and much lower Rct of 24 Ω for the hybrid anode, from 75 Ω and 86 Ω for rGO and MWCNT respectively. The dramatic increases were attributed to the reduction in rGO cross linkage from MWCNT internal stabilisation, providing a 3D nanostructure for the attachment of a greater number of bacterial cells.

However, ‘at-interface’ biohybridisation based on nanostructured electrodes require bacterial strains with some form of direct electron transfer ability. Other strategies, using nanomaterials to enable direct EET in non- or poorly electroactive organisms have been suggested. An early example of this is Rawson’s 2011 study mentioned earlier, using osmium-bipyridine functionalised SWCNTs as ‘nanoelectrodes’ capable of accepting electron flow from the surface-redox centres of Proteus vulgaris (82). In this case, ET from P. vulgaris was previously unreported in the literature. These findings are encouraging, inferring that nanomaterial biohybridisation can offer potential in conferring direct ET abilities in organisms previously considered incapable of this form of ET.

Conclusions and Future Directions

MET were first imagined over a century ago, yet their application in real-world systems is rare with only a handful of systems progressing past the laboratory scale. This is due to low power generation, partly attributable to the low efficiency of native EET mechanisms to connect cellular redox processes and the electrode of MET.

Engineering biology offers novel methods to increase the rate of bacterial EET: recombination of native EET pathways into more industrially relevant, well-characterised organisms offers potential to produce highly exoelectrogenic strains aligned with the requirements of larger-scale systems. Furthermore, the larger genetic toolkits allow the manipulation of such chassis, offering opportunities to add additional functionality to native EET pathways. Exploitation of G. sulfurreducens conductive nanowires, a major route of microbial EET, has already been demonstrated in several industrially relevant organisms. Modification of the pili monomer protein structure, via aromatic amino acid composition increases and inclusion of synthetic amino acids may offer a complementary route to the generation of a bacterial strain capable of high-rate EET. Examples using this methodology exist in the literature, with EET rates surpassing native mechanisms. While recent analysis has suggested the presence of polymerised OmcS and OmcZ cytochrome-based nanowires (83), and their structure has been confirmed via cryo-electron microscopy (84), their recombination to organisms more amenable to synthetic biology and metabolic engineering tools is yet to be achieved. This work is vital to allow the exploitation of these EET pathways in MET, as the growth requirements of their native Geobacter spp hosts limit their potential in industrial-scale processes.

In contrast the recombination strategies outlined, conductive nanomaterials offer alternative methodologies to bridge the gap between microbial redox machinery and the circuitry of MET. A wide range of studies are present in the literature both enhancing native EET pathways and conferring increased exoelectrogenic abilities to poorly electroactive organisms. Increasing surface area to volume of electrode surfaces is a major area of interest. Production of highly macroporous electrodes via nanomaterial functionalisation has been shown to be effective at increasing the rate of microbial EET. Alongside this approach, the conductivity of a natively produced bacterial biofilm can be increased via doping reactor systems with conductive nanoparticles to produce a conductive scaffold throughout the system. These techniques offer the potential to optimise the EET capabilities of an industrially relevant exoelectrogenic strain. In contrast, a range of nanomaterial-cell integration systems have been suggested. By integrating conductive materials within the bacterial membrane, intracellular redox processes can be ‘wired’ to electrodes without affecting cell viability and potentially allowing the development of novel ‘biohybrid’ EET mechanisms. Comparison of the electron transfer efficiencies achieved via native and imported methods would be highly valuable in advancing research in MET, by generating a greater range of EET-capable bacterial chassis available to system architects.

Our hypothesis is that combining engineering biology and biohybrid approaches to industrially relevant organisms that can grow on cheap and renewable resources can enable the seamless design of electronic-cellular interfaces to maximise charge transfer, aiding the translational pathway of developing commercially viable MET.

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Acknowledgements

The authors thank the Nottingham-Rothamstead Doctoral Training Partnership for providing a studentship to Benjamin Myers (BB/M008770/1) and The Carbon Recycling Network (BBSRC-NIBB, BB/S009833/1) for a Proof of Concept funding awarded to Katalin Kovács and Frankie J. Rawson with industrial support from Johnson Matthey.

The Authors

Benjamin Myers is a doctoral student at The University of Nottingham, UK, working between the School of Pharmacy and Synthetic Biology Research Centre (SBRC-Nottingham). He studied Food Science BSc at the University of Nottingham and has industrial experience in analytical chemistry and environmental pollution monitoring. Ben is interested in using technological advancements to find solutions to current environmental issues. His research involves developing novel methods to electrochemically connect microbial metabolic processes to the circuitry of bioelectrochemical systems, with the aim of developing new electricity and platform chemical generation pathways under commercially viable conditions.

Phil J. Hill is an Associate Professor in Molecular Microbiology (University of Nottingham, School of Pharmacy) with a strong interest in developing systems to allow the ‘in situ’ tracking of microorganisms. These systems allow assessment of cellular metabolism or measure gene expression in real time, without destruction of the organisms under investigation. These tools have been used to track pathogens during infection, study biofilms on medical devices and for screening of biofilm removers. More recently, he has been involved in modifying the surface of bacteria to improve biofilm formation on electrodes.

Frankie J. Rawson is an Associate Professor (University of Nottingham, School of Pharmacy). He undertook Postdoctoral positions at the University of Birmingham, UK, and University of Canterbury, New Zealand. He obtained a PhD from the University of the West of England, UK, in 2009. He leads the Laboratory of Bioelectronics within the Biodiscovery Institute and has held prestigious Leverhulme Early Career (2013–2016) and Nottingham Research Fellowships (2016–2019) and received an Engineering and Physical Sciences Research Council (EPSRC) funded Healthcare Technology Challenge award in 2018. His research is focused on understanding bioelectrical activity and developing new bioelectronic tools to interface with cells and modulate their function. He is applying this research to develop new bioelectronic medicine, sustainable energy and chemical synthesis tools.

Katalin Kovács is an Assistant Professor at the University of Nottingham, School of Pharmacy to research healthcare provision in extreme and resource-limited environments using engineering biology. She has more than 10 years of experience in synthetic biology and has played a leading role in the development of synthetic biology tools and methodologies for non-model, aerobic and anaerobic organisms, with a particular focus on metabolic engineering to produce platform chemicals and high value molecules. Her current research activities include studying and exploiting the potential of hydrogen oxidising microorganisms for the sustainable production of on site, on-demand molecules from CO2 and renewable energy via microbial electrosynthesis.

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