Biohybrids for Solar Fuels: Whole-cell Photocatalysis by Non-photosynthetic Organisms

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We propose to tap into sunlight, an underutilised source of clean power, and address the direct exchange of electrons between bacterial cells and inorganic photocatalysts for the biophotocatalytic production of solar chemicals including fuels. Current state-of-the-art technology, referred to as "bionic leaf", relies on the transfer of energy via intermediates such as hydrogen. By contrast, recent results from the applicants indicate that cytochromes purified from the extracellular respiratory machinery of Shewanella oneidensis MR-1 (MR-1) enable direct exchange of solar energy with synthetic photosensitisers. The MR-1 extracellular respiratory machinery exchanges energy/electrons across the bacterial outer membrane. To this end, we propose a novel synthetic biology approach in which bespoke photocatalysts are directly coupled to the extracellular cytochromes of MR-1 in vivo. Modular biohybrid assemblies will be produced that use intracellular redox transformations to sustain light-driven extracellular catalysis thereby closing the redox loop and enabling self-sustaining production of solar fuels. Two proof-of-principle light-driven reactions are proposed: (a) MR-1 catalysed reductions, such as protons to hydrogen or carbon dioxide to formate, coupled to inorganic photo-oxidation of industrially-relevant alcohols to aldehydes, and (b) MR-1 catalysed oxidation of glycerol (a major underutilised by-product of biodiesel production) to ethanol coupled to the inorganic photo-reduction of carbon dioxide to formate.

Societal impact
The aim of this project is to use biophysical, (bio)nanotechnological and synthetic biological approaches to study Shewanella for exploitation in the area of Industrial Biotechnology and Bioenergy. In particular, we aim to couple respiratory proteins of Shewanella to inorganic photocatalysts to harvest solar energy for novel and innovative approaches to produce value added chemicals and fuels. For instance, we will explore the solar conversion of glycerol to ethanol and formate. Glycerol is a major underutilised by-product from biodiesel. Approximately 1 kg of crude glycerol is produced for every 10 kg of biodiesel, in the US, this would equate to about 0.8 x 109 kg of glycerol in 2016.
Renewable energy is recognised as a top national strategic priority (UK White Paper on Energy). Several incidents have demonstrated the fragility of the global energy supply such as the outbreak of conflicts and civil wars in the Middle-East and the ecological and humanitarian threat of a nuclear meltdown in Fukushima, Japan. The search for alternative energy sources is therefore of major GLOBAL importance. The Paris Agreement in 2015 has set out a global strategy to minimise the impact of climate change by reducing greenhouse gas emissions. A solution to this problem has to be sought by combining a multitude of complementary 'alternative' energy sources; this research will contribute to this progress.

Technological impact
The overall concept of this proposal is microbial catalysis driven by solar energy harnessed by inorganic photocatalysts. The state-of-the-art in solar-driven microbial catalytic systems first produces hydrogen and, in a second step, uses this hydrogen as an energy vector to drive downstream bioproduction of higher value compounds, e.g. reduction of CO2 to fusel alcohols by Ralstonia. This proposal aims to advance the state-of-the-art by directly coupling the photocatalyst and microbial catalytic systems.
Our proposed research into the coupling of outer membrane proteins with inorganic photocatalysts is basic research with academic beneficiaries. However, after successful completion of this project, we envisage that our work will contribute to (a) the future design of hybrid bacterial-inorganic (photo-)catalytic systems for chemical conversions and (b) increased knowledge on the ability of Shewanella to transport electrons across the outer membrane. Conjugation between inorganic materials and biomacromolecules has wide-ranging relevance to technology, including bioenergy (as proposed here), health technology, e.g. drug delivery, and the development of novel probes for cellular localisation and trafficking. Insights from our project will also impact on biotechnology exploiting bacterial electron exchange with electrodes for which Shewanella is an important model system. Examples include; mediatorless microbial fuel cells, which run on waste carbon sources (such as in waste water) to produce electricity or hydrogen, and, selective production of reduced organic products when electrons are supplied from a cathode (microbial electrosynthesis), or, oxidised organic products when the electrons from fermentation are delivered to an anode.

Collaborations and training
This project will consolidate the recently formed partnership between Butt, Clarke (UEA), Jeuken (Leeds) and Reisner (Cambridge). The project will extent the partnership to Gralnick (USA) who will bring metabolic insight and expertise in engineering Shewanella for targeted biotransformations. Within this project we will also provide top-quality cross-disciplinary training for three BBSRC PDRAs and a research technician, to provide expertise in the development of alternative energy biotechnologies, an area of critical scientific, technological and economic importance for the future.