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. 2024 Jul 16;121(29):e2404958121.
doi: 10.1073/pnas.2404958121. Epub 2024 Jul 10.

Engineering bionanoreactor in bacteria for efficient hydrogen production

Weiming Tu  1 , Ian P Thompson  1 , Wei E Huang  1
Affiliations

Engineering bionanoreactor in bacteria for efficient hydrogen production

Weiming Tu et al. Proc Natl Acad Sci U S A. .

Abstract

Hydrogen production through water splitting is a vital strategy for renewable and sustainable clean energy. In this study, we developed an approach integrating nanomaterial engineering and synthetic biology to establish a bionanoreactor system for efficient hydrogen production. The periplasmic space (20 to 30 nm) of an electroactive bacterium, Shewanella oneidensis MR-1, was engineered to serve as a bionanoreactor to enhance the interaction between electrons and protons, catalyzed by hydrogenases for hydrogen generation. To optimize electron transfer, we used the microbially reduced graphene oxide (rGO) to coat the electrode, which improved the electron transfer from the electrode to the cells. Native MtrCAB protein complex on S. oneidensis and self-assembled iron sulfide (FeS) nanoparticles acted in tandem to facilitate electron transfer from an electrode to the periplasm. To enhance proton transport, S. oneidensis MR-1 was engineered to express Gloeobacter rhodopsin (GR) and the light-harvesting antenna canthaxanthin. This led to efficient proton pumping when exposed to light, resulting in a 35.6% increase in the rate of hydrogen production. The overexpression of native [FeFe]-hydrogenase further improved the hydrogen production rate by 56.8%. The bionanoreactor engineered in S. oneidensis MR-1 achieved a hydrogen yield of 80.4 μmol/mg protein/day with a Faraday efficiency of 80% at a potential of -0.75 V. This periplasmic bionanoreactor combines the strengths of both nanomaterial and biological components, providing an efficient approach for microbial electrosynthesis.

Keywords: Gloeobacter rhodopsin; H2 production; Shewanella oneidensis MR-1; bionanoreactor; nanomaterials.

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Conflict of interest statement

Competing interests statement:W.T., I.P.T., and W.E.H. have filed a provisional patent application with the UK Patent Office related to this work.

Figures

Fig. 1.
Fig. 1.
Schematic of the sustainable bioprocess for H2 bioproduction. S. oneidensis MR-1 uses hydrogenase to catalyze H2 synthesis from protons and electrons, powered by light and electricity. Reduced graphene oxide (rGO) and FeS nanoparticles were introduced to enhance the electron transfer. The cells were engineered to express GR and its antenna CAN, which harvest photons to pump protons from cytoplasm to periplasm.
Fig. 2.
Fig. 2.
The self-assembly of biogenic FeS nanoparticles in the periplasm of S. oneidensis MR-1. (A) A TEM image of S. oneidensis MR-1 after two-day incubation with thiosulfate and FeSO4 to form FeS nanoparticles in the periplasm and on the outer membrane. OM: outer membrane; IM: inner membrane. (B) A typical Raman spectrum of FeS nanoparticle synthesized by S. oneidensis. (C) Single-cell Raman spectra of cells of S. oneidensis with and without FeS nanoparticles. (D) Fumarate reduction test. The biocathode was poised at −0.5 V (vs. Ag/AgCl), and 25 mM fumarate was added at ~50 min.
Fig. 3.
Fig. 3.
The integration of the biogenic rGO with S. oneidensis MR-1 enhanced H2 production. (A) Raman spectra of GO and rGO resulting from the reduction reaction by S. oneidensis MR-1. (B) The biomass protein on the electrodes based on carbon paper (CP), CP with rGO, and CP with rGO and self-assembled FeS nanoparticles. (C) Average current consumption per cell and (D) H2 production over 72 h using the bioelectrode based on CP, CP with rGO, and CP with rGO and FeS nanoparticles at the cathodic potential of −0.75 V vs. SHE. Statistics were performed with Student’s t test (data are means ± SD, n = 3).
Fig. 4.
Fig. 4.
The expression of GR and CAN in S. oneidensis MR-1-GR-CAN enhanced H2 production boosted by the light. (A) The pictures of cell pellets with (GR+) and without (GR–) Gloeobacter rhodopsin expression. (B) A typical Raman spectrum of a cell with GR complex identified by a band at ~1,530 cm–1. (C) The pictures of cells pellet with (CAN+) and without (CAN–) canthaxanthin expression. (D) A typical Raman spectrum of a cell with CAN identified by a band at ~1,005, 1,155, and 1,517 cm–1. (E) Extracellular proton concentration changes in response to illumination with white light (~200 μmol/m2/s). Data are means ± SD, n = 3.
Fig. 5.
Fig. 5.
The integration of nanomaterials (rGO and FeS) and biological GR, CAN and [FeFe]-hydrogenase into the periplasmic bionanoreactor of S. oneidensis MR-1-GR-CAN-HydAB has achieved high H2 production. (A) The response of the engineered S. oneidensis MR-1-GRCAN to light and dark. (B) H2 production by dead S. oneidensis WT cells (after 15-min 110 °C heat inactivation), WT cells, WT cells (dead) with nanomaterial engineering, WT cells (live) with nanomaterial engineering, the engineered S. oneidensis MR-1-GR-CAN with GR-CAN, and the engineered S. oneidensis MR-1-GR-CAN-HydAB with GR-CAN and the overexpression of hydrogenase, at the potential of −0.75 V vs. SHE under illumination. Statistics were performed with Student’s t-test (data are means ± SD, n = 4).
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