Semi-Artificial Photosynthesis with Wired Enzymes

Project Information

MatEnSAP

Grant agreement ID: 682833

DOI

10.3030/682833

Project closed

EC signature date 23 April 2016

Start date 1 October 2016

End date 31 March 2023

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 1 960 289,00

EU contribution

€ 1 960 289,00

Coordinated by

THE CHANCELLOR MASTERS AND SCHOLARS OF THE UNIVERSITY OF CAMBRIDGE
United Kingdom

Periodic Reporting for period 4 - MatEnSAP (Semi-Artificial Photosynthesis with Wired Enzymes)

Reporting period: 2021-04-01 to 2023-03-31

Summary of the context and overall objectives of the project

The motivation of this research is to develop new toolsets for driving energy demanding (endergonic) chemical reactions with sunlight via a new interdisciplinary approach: semi-artificial photosynthesis. We focus on the study of solar-to-fuel conversion reactions since they form the basis of renewable fuel generation, which is urgently needed to reduce greenhouse gas emissions and provide a practical route of storing solar energy.

Currently, solar fuel conversion is studied via ‘artificial photosynthesis’, which utilises solely synthetic, often biomimetic, components to convert and store solar energy, but is often constrained by inefficient catalysis as well as costly and toxic materials. Nature, on the other hand has already produced many bio-catalysts that can efficiently and selectively perform thermodynamically and kinetically demanding multi-electron transformations, which drive life-sustaining reactions such as photosynthesis. Semi-artificial photosynthesis bridges the rapidly developing fields of synthetic biology and artificial photosynthesis, and is an unexplored platform for understanding solar fuel generation.

The objectives of this research are to: 1) develop the toolbox (in the form of for example: electrodes, redox connections, and complementary photosensitisers) needed for bridging artificial and biological photosynthesis; 2) modify and develop techniques that can be used in a complementary manner to provide a holistic picture of the biotic-abiotic interface, and thus aid rational design in semi-artificial photosynthesis; and 3) produce novel and efficient proof-of-concept solar fuel generation pathways that cannot be accessed via artificial or natural photosynthesis alone.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

Aim 1 aims to establish the toolbox needed to interface the biotic with the abiotic components:
i) We expanded current state-of-the-art ITO electrode design to TiO2 and graphene and allowed for the incorporation of live cells [J. Am. Chem. Soc., 2018, 140, 6-9; Nano Lett., 2019, 19, 1844-1850; Angew. Chem. Int. Ed., 2019, 58, 4601-1605; Proc. Natl. Acad. Sci, 2020, 117, 5074-5080].
ii) We integrated state-of-the-art photovoltaic componements (p-Si and lead halide perovskites) with enzymes [Angew. Chem. Int. Ed., 2018, 57, 10595-10599; ACS Energy Lett., 2020, 12, 8176-8282; ACS Catal., 2021, 11, 1868-1876].

Aim 2 develops new approaches to understand the biotic-abiotic interface:
i) A Mo-containing formate dehydrogenase was characterised using a combination of inhibition studies, electrochemistry, QCM and ATR-IR spectroscopy and modelling [J. Am. Chem. Soc., 2017, 139, 29, 9927-9936; J. Am. Chem. Soc., 2020, 142, 12226-12236; Angew. Chem. Int. Ed., 2019, 58, 4601-1605]. Some of those techniques were also used to investigate the whole cell-electrode interface [J. Am. Chem. Soc., 2020, 142, 5194-5203]
ii) The protein conduit, MtrC, was identified for high performance H2O2 reduction when developing Raman spectroscopy [J. Am. Chem. Soc., 2017, 139, 9, 3324-3327].
iii) Rotating ring disk electrodes were established to study photo-induced charge conversion events by protein-films [J. Am. Chem. Soc., 2018, 140, 17923-17931].
iv) We have contributed to the development of protein film electrochemical EPR spectroscopy [Chem. Commun., 2019, 55, 8840-8843]
v) A carboxysome-inspired CO2 reduction system [Angew. Chem. Int. Ed., 2023, 62, e202218782] and a carbon dot biohybrid system [ J. Am. Chem. Soc. 2022, 144, 14207−14216] have been characterised.
vi) The orientation of enzymes on electrodes [ACS Catal., 2022, 12, 1886−1897] as well as the local environment in bioelectrochemistry has been unraveled [Proc. Natl. Acad. Sci USA, 2022, 119, e2114097119 and Nature Chem., 2022, 14, 417–424];
vii) We have contributed to the understanding of enzyme mechanisms [J. Am. Chem. Soc., 2022, 144, 18296−18304] and identification of ultra-fast quenching of Photosystem II [Nature, 2023, 615, 836-840].

Aim 3 establishes novel proof-of-concept solar fuel generation pathways via semi-artificial photosynthesis:
i) We have accomplished the wiring of enzymes for solar-driven overall bias-free water splitting and CO2 reduction [Nature Energy, 2018, 3, 944-951; J. Am. Chem. Soc., 2018, 140, 16418-16422].
ii) Reversible interconversion of formate into H2/CO2 has been accomplished with a pair of wired redox enzymes (J. Am. Chem. Soc., 2019, 141, 17498-17502]
iii) Semi-artificial devices and systems have been assembled: simultaneous CO2 and cellulose to formate conversion [Angew. Chem. Int. Ed., 2023, 62, e2022158]; simultaneous CO2 and plastic upcycling [Nature Synth., 2023, 2, 182–192]; microbial plastic fermentation [Angew. Chem. Int. Ed. 2022, 61, e202211057]; bacteria photocatalyst sheets for CO2 utilisation [Nature Catal. 2022, 5, 633–641], solar CO2 utilisation coupled to alcohol oxidation [Nature Synth., 2022, 1, 77–86]; and a semi-artificial leave for CO2-to-formate conversion [Angew. Chem. Int. Ed., 2022, 60, 26303 –26307].
iv) The development of the semi-artificial devices has been translated into synthetic prototypes for bias-free solar fuel production: Thermoelectric-photoelectrochemical water splitting devices [J. Am. Chem. Soc., 2023, 145, 13709−13714] and the floating artificial leave [Nature, 2022, 608, 518–522].
vi) The insights from this ERC project have resulted in a bio-electrocatalytic platform for food waste upcycling [ACS Catal., 2023, 12, 13360−13371] as well as synthetic ligand tuning on quantum dots for CO2 reduction [Chem. Sci, 2022, 13, 5988–5998 and Chem. Sci., 2021, 12, 9078–9087].

Reviews: Acc. Chem. Res., 2019, 52, 1439-1448; Nat. Rev. Chem., 2020, 4, 6-21; Nature Nanotechn., 2018, 13, 890-899; Chem. Soc. Rev., 2020, 49, 4926-4952; Acc. Chem. Res., 2022, 55, 3376−3386; Nature Catal., 2023, 6, 657–665; Nature Rev. Methods Primers, 2023, 3, 61.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

The three goals of the project have been achieved to establish semi-artificial photosynthesis for solar fuel production. As for the combination of biological catalysts with synthetic materials (aim 1), we have successfully integrated isolated enzymes with semiconductors, conducting metal oxides, 3D electrode architectures, polymers and synthetic dyes as proposed. We have also shown the possibility to use state-of-the-art light absorbers from the photovoltaics field such as silicon and perovskites for semi-artificial photosynthesis and combine live (photosynthetic and non-photosynthetic) bacteria with metal oxide electrodes, allowing potentially the more efficient synthesis of more complex organic products with improved stability in the future.

As for the development of techniques to investigate the enzyme-electrode interface (aim 2), we have demonstrated the usefulness of advanced electrochemistry (e.g. rotating ring disk electrochemistry; photoelectrochemistry), advanced vibrational spectroscopy (IR and Resonance Raman spectroscopy), confocal fluorescence spectroscopy, quartz crystal microbalance with dissipation and, in collaboration, time-resolved spectroscopy and protein film electron paramagentic resonance spectroscopy. We have also elucidated the importance of the local environment and its influence on the performance of our hybrid electrodes.

We have established multiple bias-free solar H2 production and CO2 reduction systems using semi-artificial photosynthesis using enzyme cascades or live cells (aim 3), and also used this platform to achieve artificial photosynthesis using solely synthetic components.

Schematic representation of semi-artificial photosynthesis