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Dual-channel energy pathway combining energy molecule supply and electron transfer to support solar-to-chemical production in an E. coli–thylakoid hybrid

Abstract

Achieving high yields of chemicals via biosynthesis is desirable but challenging because only a small amount of energy molecules (such as adenosine triphosphate (ATP), reduced nicotinamide adenine dinucleotide (NADH) and reduced nicotinamide adenine dinucleotide phosphate (NADPH)) within microorganisms are utilized for target chemical production. Drawing inspiration from the ability of plant-derived thylakoid to convert solar energy into energy molecules, an Escherichia coli–thylakoid hybrid with a dual-channel energy pathway combining energy molecule supply and electron transfer was created by implanting thylakoid in E. coli. Under light, photoelectrons produced in thylakoid were directly utilized to synthesize ATP and NADPH, which were then supplied to E. coli. Photoelectrons from thylakoid can transport and be captured by redox mediators, elevating the level of ATP and NADPH by facilitating the electron transport chain of E. coli. This dual-channel energy pathway boosted the level of energy molecules, enabling the E. coli–thylakoid hybrid to achieve an impressive H2 production rate of \(15.1\,{\mathrm{mmol}}\,{\mathrm{h}}^{-1}\,{\mathrm{g}}_{\mathrm{dcw}}^{-1}\) (dcw, dry cell weight), comparable to top-performing E. coli-based systems. Biogenic thylakoid presented excellent biocompatibility and the E. coli–thylakoid hybrid did not exhibit oxidative stress.

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Fig. 1: E. coli–thylakoid hybrid for solar-to-chemical production.
Fig. 2: Preparation and characterization of the E. coli–thylakoid hybrid.
Fig. 3: Dual-channel energy pathway combining energy molecule supply and electron transfer in the E. coli–thylakoid hybrid.
Fig. 4: The stability of the E. coli–thylakoid hybrid.
Fig. 5: Application of the E. coli–thylakoid hybrid in photosynthetic H2 production.
Fig. 6: Transcriptomic analyses of light-driven photosynthetic H2 production in E. coli and the E. coli–thylakoid hybrid.
Fig. 7: Schematic detailing the photosynthetic H2 production pathways in the E. coli–thylakoid hybrid.

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Data availability

All data generated in this study are provided in the Supplementary Information and Source Data files. Source data are provided with this paper.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (22134004, B.T.; 2247041268, L.L.), the Taishan Scholars Program of Shandong Province (tstp20250528, L.L.), the Natural Science Foundation of Shandong Province of China (ZR2024QB013, J.A.), the Key R&D Plan of Shandong Province (2021ZDPT01, L.L.) and the Project of Shandong Provincial Center for Fundamental Science Research (YDZX2024150, L.L. and J.A.).

Author information

Authors and Affiliations

Contributions

The project was conceptually designed by B.T., L.L. and J.A. The majority of the experiments were conducted by T.C. and J.A, assisted by F.G and W.Z. Data analysis and interpretation were done by J.A and T.C. The paper was prepared by J.A, L.L and B.T. All authors have given approval to the final version of the paper.

Corresponding authors

Correspondence to Lu Li or Bo Tang.

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The authors declare no competing interests.

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Nature Synthesis thanks Bo Wang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary handling editor: Thomas West, in collaboration with the Nature Synthesis team.

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Extended data

Extended Data Fig. 1 Characterization of thylakoid.

(a) The SDS-PAGE analysis of thylakoid. (b) Calibration curve for DCPIP. Data points are reported as mean ± standard deviation derived from 3 independent experiments (n = 3). The UV-vis absorption intensity of DCPIP in the thylakoid solutions against time under dark (c), with light irradiation (d), with light irradiation and DCMU (e). (f) UV-vis absorption spectroscopy of thylakoid after being placed for five days.

Source data

Extended Data Fig. 2 Characterization of E. coli–thylakoid hybrid.

(a) Zeta potential value of E. coli and thylakoid. Data points are reported as mean ± standard deviation derived from 3 independent experiments (n = 3). (b) The UV-vis absorption spectra of E. coli, PDA, and E. coli@PDA. (c) The UV-vis absorption spectra of the E. coli–thylakoid hybrid and E. coli. (d) The CLSM image of E. coli. (e) Bio-TEM image of thin-sectioned E. coli. (f) Bio-TEM image of thin-sectioned the E. coli–thylakoid hybrid.

Source data

Extended Data Fig. 3 Light-driven NADPH production in thylakoid.

(a) The UV-vis absorption spectra of NADPH with different concentrations. (b) Calibration curve for NADPH. Data points are reported as mean ± standard deviation derived from 3 independent experiments (n = 3). The UV-Vis absorption spectra of NADPH generated on thylakoid (40 µg Chl·mL−1) against time under dark (c) and light radiation (d) condition. (e) The UV-vis absorption spectra of NADPH generated on thylakoid (80 µg Chl·mL−1) against time under light condition. (f) The UV-vis absorption spectra of NADPH generated on thylakoid (160 µg Chl·mL−1) under light condition.

Source data

Extended Data Fig. 4 Electron transfer characteristics between thylakoid and redox mediator.

(a) Photocurrent responses of thylakoid, FAD, and physically mixed group of thylakoid and FAD. (b) Photocurrent responses of thylakoid, coenzymes Q, and mixed group of thylakoid and coenzymes Q. (c) Photocurrent responses of thylakoid and thylakoid@PDA.

Source data

Extended Data Fig. 5 H2 production rate of E. coli, E. coli–thylakoid hybrid, and E. coli–thylakoid with DCMU.

Data points are reported as mean ± standard deviation derived from 3 independent experiments (n = 3).

Source data

Extended Data Fig. 6 Stability analysis of E. coli–thylakoid.

(a) Fluorescence microscopy image of E. coli and E. coli–thylakoid hybrid after 6 h reaction under real light. Live/dead stained cells via SYTO 9 (green) and PI (red). (b) UV-vis absorption spectroscopy of thylakoid in the E. coli–thylakoid hybrid after 6 h reaction. (c) The 3-dimensional confocal laser scanning microscopy image of the E. coli–thylakoid hybrid after 6 h reaction.

Source data

Extended Data Fig. 7 Glucose consumption of E. coli and the E. coli–thylakoid hybrid at different reaction times under light.

Data points are reported as mean ± standard deviation derived from 3 independent experiments.

Source data

Extended Data Table 1 Fitting parameters for the fluorescence decay curves of thylakoid and the E. coli–thylakoid hybrid
Extended Data Table 2 Comparation of the H2 production rate of the E. coli–thylakoid hybrid and various semiconductor–microorganism systems

Supplementary information

Supplementary Information

Supplementary Methods and Tables 1–5.

Reporting Summary

Source data

Source Data Fig. 2

Unprocessed TEM, SEM and CLSM; UV–vis and flow cytometry.

Source Data Fig. 3

UV–vis, I-T EIS, time-resolved spectroscopy, energy cofactor generation test and Single-molecule fluorescence imaging.

Source Data Fig. 4

Unprocessed SEM and CLSM; UV–vis, ROS test and biocompatibility test.

Source Data Fig. 5

Hydrogen production rate under xenon lamp and sunlight.

Source Data Fig. 6

Transcriptome analysis.

Source Data Extended Data Fig. 1

Unprocessed gel; DCPIP reduction and thylakoid stability.

Source Data Extended Data Fig. 2

Unprocessed CLSM and bio-TEM; zeta potential and UV–vis.

Source Data Extended Data Fig. 3c

UV–vis of NADPH reduction.

Source Data Extended Data Fig. 4

Photocurrent test.

Source Data Extended Data Fig. 5

DCMU inhibits hydrogen production.

Source Data Extended Data Fig. 6

Unprocessed CLSM; UV–vis.

Source Data Extended Data Fig. 7

Glucose consumption result.

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An, J., Chen, T., Ge, F. et al. Dual-channel energy pathway combining energy molecule supply and electron transfer to support solar-to-chemical production in an E. coli–thylakoid hybrid. Nat. Synth 4, 1408–1421 (2025). https://doi.org/10.1038/s44160-025-00853-0

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