Electricity is one of the most widely available forms of energy and can be produced abundantly and sustainably. Microbial electrosynthesis is a new research field, in which renewable electricity can be used to drive microbial production processes. This allows commodity chemicals to be produced by electrically tapping into the plethora of useful biofuels and biochemicals that microorganisms can make.
By Dr K. Rabaey, Dr A. Johnstone, Dr A. Wise, Dr S. Read and Dr R. A. Rozendal
Breathing minerals to survive
To understand how microorganisms can use or produce electrical current, we need to understand how they deal with electrons. All living organisms gain energy by oxidising an electron donor and reducing an electron acceptor, hence life is driven by electrochemistry. The resulting electron flow, over a potential difference,
provides effective power (Watts) to the organism. Typically, organisms will use this power to generate ATP and NAD(P)H, the universal energy and electron carriers for cells. Exactly 100 years ago, it was recognised that microorganisms can link this electrical “circuit” to the outside of the cell – microorganisms achieved the reduction of an electrode (platinum wire) in their environment. In the late 80s it was discovered that microorganisms effectively manage to transport electrons out of the cell, enabling them to use solid minerals as an electron sink. The concept of
“extracellular electron transfer” was born.
Extracellular electron transfer (EET) refers to the transport of electrons in and out of the cell, in order to support microbial respiration. Most widely studied is the microbial reduction of solid-state electron acceptors, such as iron and manganese oxides, and also electrodes. These mineral conversions are crucial for the biogeochemical cycles in nature. There are two main strategies for EET, namely direct and indirect transport [1]. Direct transport involves membrane-associated protein complexes, predominantly cytochromes, and potentially also nanowires. The latter have been discovered only recently; essentially they are conductive pili (“wires”) produced by the cell, in order to transport electrons from the cell to the mineral – or an electrode. The cell is indeed wiring up to its solid electron acceptor. Indirect transport involves the production or use of soluble molecules that can transport the electrons to and from the cell. These molecules are called “electron shuttles”, and examples are phenazines, humics and sulfur species. It is important to understand that while many organisms have the capability to perform EET, not many are truly successful – therefore, assisting microorganisms by providing them with electron shuttles provides a means to artificially achieve EET. In addition, it has been shown that long term culturing of mixed populations or pure cultures lead to increased capability
in electron transfer [Figure 1].
From minerals to electrodes
Interestingly, long before the role of EET in biogeochemical cycles was discovered, it was observed that microorganisms can interact with electrodes. The interaction most studied is that with an anode, where microorganisms can catalyse the oxidation of organics to carbon dioxide, protons and electrons. Such an electrode is called a bioanode and if linked to a cathode (where reduction occurs), a biocatalysed electrochemical system is created. As early as 1962, Davis and Yarbrough used this concept to develop the “microbial fuel cell”, capable of using organic substrate for the production of electrical power [2]. Indeed, linking microbial metabolism to a low potential anode and then conveying the harvested electrons to a high potential cathode generates net electrical power from the microbial decomposition of organic matter [Figure 2A]. This concept has gained considerable momentum in the past few years, due to the interest in microbial fuel cells for energy recovery from wastewater [3]. There are also niche applications, such as electricity generation at remote locations, powered by the microorganisms in marine sediments.
In 2003, microbial electrolysis cells were first described. If current is applied to the system instead of extracted, the cathode potential can be driven sufficiently low to electrolyse water [Figure 2B]. This allows (i) hydrogen gas to be indirectly produced from any organic feedstock and (ii) hydrogen production at far lower energy requirements than conventional electrolysis [4].
As anodes and cathodes can provide a highly controllable source of oxidising or reducing power, respectively, they are increasingly used for the biodegradation
of recalcitrant xenobiotics or nuisance compounds. Examples of cathodic reduction processes are the removal of nitrobenzene, azo dyes, nitrate and perchlorate, while anodic oxidation was used for the removal of 1,2-dichloroethane and sulfur species.
Coming up – next generation bioelectrochemical systems
Based on the microbial fuel cell and microbial electrolysis cell concepts, a number of bioelectrochemical production processes were recently put forward. An ion-selective membrane typically separates the anode and cathode. In most cases, a cation exchange membrane is used, allowing cations to travel from anode to cathode while anions (like acetate) are retained at the anode. While about one proton is produced for every electron going into the electrical circuit, there are at present no membranes that can transport only protons towards the cathode. The cross-over of other cations such as sodium causes a decreasing pH in the anode, and increasing pH at the cathode. Recently, this was exploited to produce alkaline solutions at the cathode [5]. This would enable (mainly industry) to produce caustic on site, using the organics available in the wastewater as driver. As a side effect, cations such as sodium and potassium are removed from the wastewater, leading to lower salt discharges in the environment. Similarly, the observation that oxygen reduction at cathodes often leads to hydrogen peroxide formation has now enabled a new process for the production of peroxide from wastewater. It can be expected that a whole range of microbial production processes, driven by bioelectrochemical current generation, will evolve in the coming years.
Coming up – microbial electrosynthesis Non-fossil fuel-based production of
fuels and chemicals is critical to their future supply. There are two key aspects of importance:
(i) Electricity can now be produced virtually anywhere, in a sustainable manner. However, electricity is difficult to store at high density.
(ii) Microorganisms can use a tremendous variety of organic or inorganic electron donors to produce a plethora of desirable biofuels or biochemicals.Considering the two above points, it is clear that a process linking electrical current to product formation is of considerable interest. This observation has led to a new field of research: microbial electrosynthesis. This field addresses the use of microorganisms as catalysts on cathodes (i.e., biocathodes) to achieve electricity-driven synthesis of chemicals and fuels. Recently, the first study linking solar electricity to product formation, starting from CO2, was published [6].
While not always labelled this way, microbial electrosynthesis has been around for several decades. The first demonstration involved the use of an electrical current to increase the glutamic acid yield during fermentation of glucose. Since then, the use of an electrical current to modify fermentation pathways has been the main focus. For example, butanol or propionate was produced at higher yields during glucose fermentation when an electrical current reduced the medium. In most cases, the link between the electrode and the microorganisms was established by adding a mediator, such as methyl viologen. The question, though, is whether electrons were effectively transported inside the cell, or NADH regeneration was hampered by the provided reducing power. In-depth analysis of microbial metabolism and physiology in this context is warranted.
Rather than modifying fermentation pathways, Greg Zeikus’ group used an electrical current as the sole driver of microbial respiration. For example, they reduced fumarate to succinate at high efficiency by providing Actinobacillus succinogenes with electrical current and neutral red as electron shuttle. Cathodes can, as suppliers of electrons, be compared with hydrogen gas as an electron donor. A wide range of microbial conversions driven by hydrogen, such as biopolymer production from CO2, and reduction of fatty acids to alcohols, are coming into the picture.
New perspectives for old processes
Microbial electrosynthesis has been a dormant field for several decades. Pivotal for the development seen in the past few years were the discoveries that microorganisms can directly transfer electrons to electrodes, that they develop multilayered structures (biofilms) and that they improve over time when properly enriched. In the slipstream of the microbial development, improved reactor designs and the use of new materials have enabled the development of microbial fuel cells and microbial electrolysis cells to the pilot stage. While several hurdles are yet to be overcome, it appears that this technology will find its way to the market in the coming years. The development of microbial electrosynthesis will greatly benefit from these industrial applications. The main hurdle today is again microbiology. The pathways for electron transfer towards microorganisms are poorly understood, and also the impact of material structure (topography) and properties (functional groups, charge density) needs considerable attention by researchers. Once a suitable interface between the cathode and the microorganisms is established, the existing technology can quite easily be adapted for bioproduction.
One particularly interesting development will be the direct link between solar power and bioproduction. Microbial electrosynthesis principally allows the production of biofuels and biochemicals directly on site from solar power. Hence, a method is created to generate valuable products, storing the solar power and making it transportable due to the high energy density that can be achieved. Based on energy densities of microbial photosystems and engineered solar technology, production yields per hectare per annum are potentially an order of magnitude higher than the existing alternatives such as algal fuels and particularly plant-based biofuels. Conversely, this development may boost the installation of solar panels, particularly in remote areas from which at present the transport of electricity is not economically feasible.
References
1. Rabaey K et al. Microbial ecology meets electrochemistry: electricity-driven and driving communities. ISME 2007; 1:9-18.
2. Davis JB, Yarbrough HF. Preliminary experiments on a microbial fuel cell. Science 1962; 137:615-616.
3. Logan B et al. Microbial fuel cells: methodology and technology. Environ Sci Technol 2006; 40:5181 -5192.
4. Logan B. et al. Microbial Electrolysis Cells for High Yield Hydrogen Gas Production from Organic Matter. Environmental Science & Technology 2008; 42:8630-8640.
5. Rabaey K et al. High current generation coupled to caustic production using a lamellar bioelectrochemical system. Environ Sci Technol 2010; 44 4315-4321.
6. Nevin KP. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. 2010. mBio 1:e00103-10. doi:10.1128/mBio.00103-10.
7. Rozendal RA et al. Towards practical implementation of bioelectrochemical wastewater treatment. Trends in Biotechnology 2008; 26:450-459.
Acknowledgements
The research relating to this manuscript is supported by the Australian Research Council (ARC DP0879245) (KR), by a UQ Foundation Research Excellence Award (KR) and a UQ Postdoctoral Research Fellowship (RAR).
The authors
Korneel Rabaey*, Angela Johnstone,
Alexander Wise, Suzanne Read,
René A Rozendal
Advanced Water Management Centre
The University of Queensland
Brisbane QLD4072, Australia
*Corresponding author
email: k.rabaey@uq.edu.au
