Microbial electrosynthesis for sustainable bioproduction

© Matthew Ragen

Arpita Bose, PhD, Associate Professor at Washington University, shows how microbes can be essential to the development of sustainable technologies in our pursuit of a greener economy

Photosynthesis is believed to have evolved 3.5 billion years ago. Some of the earliest phototrophs, known as photoferrotrophs, used dissolved iron as an electron source to drive photosynthetic carbon dioxide (CO2) fixation. Billions of years later, we have learned a lot about these microbes and their vital role in ancient and modern environments.

Electricity guzzling microbes

Photoferrotrophs capture electrons from reduced iron via extracellular electron uptake (EEU) and use these electrons to drive essential cellular processes (e.g. photosynthesis). With the help of the phototrophic model Rhodopseudomonas palustris TIE-1 (TIE-1), we have characterized the phototrophic iron oxidation (pio) gene cluster, which is essential for the EEU, and the proteins that encode electrons. (1) Additional work linked EEU to photosynthetic CO2 fixation in TIE-1. (2)

While we continue to deepen our understanding of EEU in TIE-1, other EEU-capable bacteria are waiting to be discovered. We have recently shown that EEU is predominant in marine anoxygenic phototrophic bacteria (3), and ongoing work in our laboratory is trying to identify more EEU-capable microbes and characterize the molecular mechanisms responsible for this process. We suspect that these “electrotrophs” are ubiquitous in nature and that new mechanisms of electron uptake must be discovered. (4)

EEU: A Catalyst for Microbial Electrosynthesis

EEU is not limited to photoferrotrophy; various bacteria can access electrons from hydrogen gas, hydrogen sulfide, iron minerals and balanced electrodes. (4) EEU can be used for the production of organic raw materials through microbial electrosynthesis (MES). (5) In MES, CO2 is converted into organic carbon compounds using electrotrophs as biocatalysts. This takes place in a bioelectrochemical system consisting of a reactor with anode and cathode in an electrically conductive bacterial growth medium. In the case of the photosynthetic EEU, MES uses renewable inputs: light, CO2 and electricity. Consequently, photosynthetic electrotrophs like TIE-1 are promising biocatalysts for sustainable MES. In addition, due to its metabolic plasticity and genetic availability, TIE-1 is a promising organism for both basic research and industrial applications. (5)

How is MES used?

To date, six main products have been created via MES:

• Acetic acid.
• Ethanol.
• n-butyric acid.
• n-butanol.
• Hexanoic acid.
• n-hexanol. (6)

Our lab used TIE-1 to make biofuel (n-butanol) (7) and bioplastic (polyhydroxybutyrate) via MES. (8) We achieved the former by introducing the n-butanol biosynthetic pathway in TIE-1 and further improving production by eliminating the electron-consuming nitrogen fixation pathway. Coupled with a bioelectrochemical platform that uses electricity generated by solar cells, we have achieved efficient biofuel production. This lays the foundation for a climate-neutral synthesis of n-butanol using sustainable resources. We also examined TIE-1’s ability to produce bioplastic (polyhydroxybutyrate, or PHB), which acts as an intracellular carbon and energy reserve for bacteria.

PHBs offer a promising alternative to petroleum-based plastics; they are heat-resistant, moldable, biocompatible and biodegradable polyesters that have been used in areas such as agriculture, aerospace, biomedicine, infrastructure and electrical engineering. It is important that the PHB production via MES with TIE-1 is based on renewable resources and not on fossil fuels. (8th)

MES has benefits beyond bio-raw materials, including biological remediation, water desalination, and other areas that have yet to be considered. Research to perfect these applications is a critical requirement for industrial applications.

Improve MES

Academic research has focused on cathode modifications, the biology of the EEU, and the isolation of electrotrophs from the environment. Our laboratory has shown that modifying electrodes with iron-based composites can increase EEU. With an immobilized iron-based redox mediator called Prussian blue, we achieved a 3.8-fold increase in cathodic current consumption. (9) We also synthesized a composite of magnetite nanoparticles and reduced graphene oxide, which we electrodeposited onto a carbon felt cathode. (10)

This resulted in 5 times higher EEU and 4.2 times higher PHB production compared to unmodified carbon felt – 20 times higher than unmodified graphite. From a biological point of view, genetically engineered strains will be a powerful tool. “Designer” strains that lack resource-consuming metabolic pathways, overexpress raw material biosynthetic pathways or express various EEU proteins from other organisms can further increase yields and efficiency. Finally, bioprospecting for new EEU-compatible strains will further expand our biological toolbox.

Which challenges remain?

The primary question is that of scalability: How do we transfer this from the laboratory to the industry and thereby strike a balance between cost and performance? EEU efficiency is a bottleneck; low electron uptake means low product formation, and current densities in excess of 50-100 mA cm-2 may be required for most MES applications. (6)

Biofilms also play an important role in achieving higher current densities; Advances in 3D printed biofilms can maximize EEU efficiency by taking into account parameters such as biofilm thickness, density and spatial organization. A mathematical modeling of MES is currently lacking and could clarify the electrochemical and biological dynamics, which leads to improved reactor designs. In addition, bioprospection, genetic engineering and synthetic biology will produce novel strains with improved EEU capabilities and resistance to various conditions. The latter is especially important as temperature, salinity, pressure, and pH all play important roles in determining MES efficiency. Changes in the design of bioreactors require strains that can tolerate these conditions.

Work towards a circular economy and a sustainable future

The latest report from the Intergovernmental Panel on Climate Change is open: Climate change is “widespread, rapid and intensifying” and mitigating global warming requires “limiting cumulative CO2 emissions to at least zero net CO2 emissions” and the reduction of other greenhouse gases. (11) Plastic waste poses a similar challenge, with global plastic volume reaching ~ 6.3 billion megatons in 2015 and expected to reach 12 billion megatons by 2050. (12) Innovations that bring us closer to a circular economy can address these challenges.

The goal of a circular economy is to minimize negative externalities and waste by using a system-level economic organization approach that takes into account the flow of renewable and non-renewable materials. This framework forces us to consider the broader impacts of MES technologies at the system level (e.g., implementing an MES platform on an industrial scale simply shifts emissions from plastics production to raw material or water use?) While MES has a role in that Decarbonization should play, Without careful consideration of external effects, there will be no truly sustainable solutions. Nonetheless, MES should be part of our toolbox when we rethink existing manufacturing pipelines.

Eric Conners, a PhD student in the Bose lab, wrote this feature.

References

1. Gupta, D. et al. Photoferrotrophs produce a PioAB electron conduction for extracellular electron uptake. mBio 10 (2019).
2. Guzman, MS et al. The phototrophic extracellular electron uptake is associated with the carbon dioxide fixation in the bacterium Rhodopseudomonas palustris. Nature communication 10, 1-13 (2019).
3. Gupta, D. et al. Photoferrotrophy and phototrophic extracellular electron uptake are common in the marine anoxygenic phototrophic Rhodovulum sulfidophilum. The ISME Journal, 1-15 (2021).
4. Gupta, D., Guzman, MS & Bose, A. Extracellular electron uptake by autotrophic microbes: physiological, ecological, and evolutionary implications. Journal of Industrial Microbiology & Biotechnology: Official Journal of the Society for Industrial Microbiology and Biotechnology 47, 863-876 (2020).
5. Karthikeyan, R., Singh, R. & Bose, A. Microbial electron uptake in microbial electrosynthesis: a mini-review. Journal of Industrial Microbiology and Biotechnology 46, 1419-1426 (2019).
6. Jourdin, L. & Burdyny, T. Microbial Electrosynthesis: Where Do We Go From Here? Trends in Biotechnology (2020).
7. Bai, W., Ranaivoarisoa, TO, Singh, R., Rengasamy, K. & Bose, A. n-Butanol production by Rhodopseudomonas palustris TIE-1. Communication biology (accepted), DOI-10.1038 / s42003-021-02781-z.
8. Ranaivoarisoa, TO, Singh, R., Rengasamy, K., Guzman, MS & Bose, A. On the way to sustainable bioplastics production with the photoautotrophic bacterium Rhodopseudomonas palustris TIE-1. Journal of Industrial Microbiology and Biotechnology 46, 1401-1417 (2019).
9. Rengasamy, K., Ranaivoarisoa, T., Singh, R. & Bose, A. A cathode coated with an insoluble iron complex improves direct electron uptake by Rhodopseudomonas palustris TIE-1.
10. Rengasamy, K., Ranaivoarisoa, T., Bai, W. & Bose, A. Magnetite-nanoparticle-anchored graphene cathode improves the microbial electrosynthesis of polyhydroxybutyrate by Rhodopseudomonas palustris TIE-1. Nanotechnology 32, 035103, doi: 10.1088 / 1361-6528 / abbe58 (2020).
11. IPCC. Climate change 2021: The physical-scientific basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press (2021).
12. Statistics. Plastic waste worldwide – statistics & facts, (2021).

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© 2019. This work is licensed under a CC BY 4.0 license.

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