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Maximizing light-driven CO2 and N2 fixation efficiency in quantum dot–bacteria hybrids

Nature Catalysis volume 5, pages 1019–1029 (2022)Cite this article

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Abstract

Integrating light-harvesting materials with microbial biochemistry is a viable approach to produce chemicals with high efficiency from air, water and sunlight. Yet it remains unclear whether all photons absorbed in the materials can be transferred through the material–biology interface for solar-to-chemical production and whether the presence of materials beneficially affects microbial metabolism. Here we report a microbe–semiconductor hybrid by interfacing the CO2- and N2-fixing bacterium Xanthobacter autotrophicus with CdTe quantum dots for light-driven CO2 and N2 fixation with internal quantum efficiencies of 47.2% ± 7.3% and 7.1% ± 1.1%, respectively, reaching the biochemical limits of 46.1% and 6.9% imposed by the stoichiometry in biochemical pathways. Photophysical studies suggest fast charge-transfer kinetics at the microbe–semiconductor interfaces, while proteomics and metabolomics indicate a material-induced regulation of microbial metabolism favouring higher quantum efficiencies compared with biological counterparts alone.

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Fig. 1: Microbe–semiconductor hybrids for efficient photocatalytic fixation of CO2 and N2.
Fig. 2: The photocatalytic performance and physical interfaces of the microbe–semiconductor hybrids.
Fig. 3: Photophysical characterizations of the microbe–semiconductor interface.
Fig. 4: Proteomic and metabolomic analyses of the photocatalytic hybrids.

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Data availability

The proteomic and metabolomic data generated in this study are available in the Supplementary Data files. The reference proteome of X. autotrophicus was obtained from the UniProt database (UP000305131), and the pathway analyses were performed based on the KEGG database (https://www.genome.jp/kegg/). Other data that support the plots within this paper and other findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank S. Tenney for the quantum yield characterization experiment, D. Xiang and B. Natinsky for the gas chromatography and A. Xiao for coding assistance. We thank E. Sletten at UCLA for the use of the fluorometer and the dynamic light scattering instrument. We also thank the UCLA Molecular Instrumentation Center, the UCLA Metabolomics Center, the UCLA Proteome Research Center and the UCLA California NanoSystems Institute for instrumental support. This study was supported by National Institutes of Health grant R35GM138241 (C.L.), the Jeffery and Helo Zink Endowed Professional Development Term Chair (C.L.), National Institutes of Health grant S10OD016387 (J.O.P.), a Hellman Fellowship (J.O.P.) and a UCLA Summer Mentored Research Fellowship (X.G.).

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Authors and Affiliations

  1. Department of Chemistry and Biochemistry, University of California Los Angeles, Los Angeles, CA, USA

    Xun Guan, Timothy L. Atallah, Yongchao Xie, Shengtao Lu, Bocheng Cao, Jingwen Sun, Ke Wu, Xiangfeng Duan, Justin R. Caram & Chong Liu

  2. Department of Chemical and Biomolecular Engineering, University of California Los Angeles, Los Angeles, CA, USA

    Sevcan Erşan & Junyoung O. Park

  3. School of Physical Science and Technology, ShanghaiTech University, Shanghai, China

    Xiangchen Hu & Yi Yu

  4. Department of Chemistry and Biochemistry, Denison University, Granville, OH, USA

    Timothy L. Atallah

  5. Department of Materials Science and Engineering, University of California Los Angeles, Los Angeles, CA, USA

    Bocheng Cao & Yu Huang

  6. California NanoSystems Institute, University of California Los Angeles, Los Angeles, CA, USA

    Yu Huang, Xiangfeng Duan & Chong Liu

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Contributions

C.L. supervised the project. C.L. and X.G. designed the experiments and wrote the manuscript. S.E conducted the metabolomic experiments and analysed the data under the supervision of J.O.P. X.H. performed the electron microscopy characterizations under the supervision of Y.Y. T.L.A. led the lifetime measurements under the supervision of J.R.C. Y.X. assisted the proteomics analysis. S.L. conducted the flow-cytometry characterization. B.C. assisted with sample preparation for electron microscopy characterization under the supervision of X.D. and Y.H. J.S. and K.W. assisted in the microbial inoculation and photocatalytic experiments. All the authors discussed the results and assisted during the manuscript preparation.

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Correspondence to Chong Liu.

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Extended data

Extended Data Fig. 1 Characterizations of CdTe quantum dots (QDs).

a, HAADF-STEM image of aggregated QDs and the corresponding EDS mapping in the same region for (b) cadmium (Cd) and (c) tellurium (Te). d, HRTEM image of individual CdTe QDs. e, Magnified HRTEM image of the highlighted region in d. f, the corresponding Fourier transform results indicate a lattice spacing of 0.21 nm, agree with the (220) plane of the cubic phase. g, Ultraviolet-visible spectrum (black) overlayed with the emission spectrum (yellow) of CdTe QDs. h, The measurement of dynamic light scattering along with the corresponding size distribution. The experiment of electron microscopy has been repeated independently for more than 3 times with similar results. Scale bars are 30 nm in a-c, 10 nm in d, and 1 nm in e.

Extended Data Fig. 2 Viability results of X. autotrophicus measured by flow cytometry.

a, The gate of X. autotrophicus in the forward-scattered light area/side-scattered light area (FSC-A/SSC-A) plot. b, Fluorescent intensity of SYTO 9 stained (live) X. autotrophicus versus its FSC-A. c, Viability percentage of the microbes under different conditions, n = 3 biological replicates with 10,000 particles recorded before gating (error bars present the standard deviation).

Extended Data Fig. 3 Gas composition analysis of reactors’ headspace by gas chromatography.

Gas chromatograms of photoreactors’ headspace for the microbe–semiconductor hybrids before (light blue) and after (dark blue) a 4-day photocatalytic reaction, along with a standard sample (black) containing O2 and H2 (0.5 v/v% for each component in N2).

Extended Data Fig. 4 Electron microscopy images of the microbe–semiconductor hybrids and controls.

a, HRTEM image of the microbe–semiconductor hybrid. b, The magnified image of the red box in a. c, The magnified image of the red box in b. d, The corresponding Fourier transform results of c indicating a lattice spacing of 0.22 nm for the QDs. e, TEM image of the microbe–semiconductor hybrid. f, The magnified image of the red box in e. g, HAADF-STEM image of sectioned microbe–semiconductor hybrid in the absence of cysteine. h, HAADF-STEM image of sectioned pure microbes. The experiment of electron microscopy has been repeated independently for more than 3 times with similar results. Scale bars are 1 μm in a, 20 nm in b, 500 nm in e, 50 nm in f, and 200 nm in g and h.

Extended Data Fig. 5 Absorption and emission spectra of partially aggregated CdTe QDs.

Absorbance (solid lines) and photoluminescence (PL) (dashed lines) spectra of the well-dispersed QD suspension (black) and the partially aggregated CdTe QDs (yellow). The average particle diameters from the dynamic light scattering measurements are 4.02 ± 0.61 and 62.06 ± 0.18 nm for the well-dispersed and partially aggregated QDs (mean + /− standard deviation), respectively.

Extended Data Fig. 6 Interactions between QDs and microbes studied by flow cytometry.

a and b, Dispersion of pure CdTe QDs. c and d, Microbial culture of X. autotrophicus. The microbe–semiconductor hybrids at (e and f) t = 0 hr and (i and j) t = 24 hrs after assembly. The mixture of QDs and microbes at (g and h) t = 0 hr and (k and l) t = 24 hrs after assembly. a, c, e, g, i, and k are the plots of SSC-A versus FSC-A that illustrate the identity of the microbial population. b, d, f, h, j, and l are the plots of emission at 525 ± 50 nm versus FSC-A that illustrate the distribution of microbial population gated in the SSC-A/FSC-A plot attached with emissive QDs. The circles in the plots illustrate the gated areas corresponding to the microbial populations attached with emissive QDs whose temporal trends were shown in (m). Representative results presented above (n = 3 biological replicates with 10,000 particles recorded before gating, error bars present the standard deviation). Additional quantification of the percentage of QDs closely interacting with microbes are available in Supplementary Fig. 4.

Extended Data Fig. 7 Stern–Volmer study for the mixture of CdTe QDs and cysteine.

The ratios of PL emission intensities of CdTe QDs (I0/I) without and with the addition of different equivalents of cysteine (Cys). A linear relationship was observed at low Cys equivalents, demonstrating a dynamic quenching mechanism orientated from the diffusive encounters between the Cys molecules and the emissive QDs. The saturated values of I0/I under high Cys equivalents due to quencher accessibility are consistent with the literature report64.

Extended Data Fig. 8 Schematic illustrations of the discussed pathways and the relevant metabolic regulations.

The regulation of the (a) Calvin–Benson-Bassham cycle, (b) two-component regulatory system, and (c) oxidative phosphorylation in the Hybrid compared to the H2-fed microbes.

Extended Data Fig. 9 The optical absorbance of the CdTe QDs in the hybrids as a function of microbial inoculation.

The optical absorbances of the CdTe QDs in the microbe–semiconductor hybrids (ODQDs), sensitive to the presence of microbial scattering centers, are plotted against the amounts of microbial inoculation presented as OD600. See section “Analytical procedures for the aliquoted samples in the photosynthetic experiments” in the Methods for details.

Extended Data Table 1 Literature reported internal quantum yields (IQYs) of biochemical fixation of CO2 and N2 powered by natural and artificial light-absorbers
Full size table

Supplementary information

Supplementary Information

Supplementary Notes 1–3, Methods, Table 1, Figs. 1–4 and references.

Reporting Summary

Supplementary Data 1

LC-MS results of the metabolome in the X. autotrophicus–CdTe hybrid system before and after the 15N and 13C isotope-labelling experiment.

Supplementary Data 2

Heatmap data for significantly regulated proteins and metabolites in the microbe–semiconductor hybrids in comparison to the H2-fed microbes.

Supplementary Data 3

LC-MS results of the proteome in X. autotrophicus under different experimental conditions.

Supplementary Data 4

Fold changes of protein expression comparing the microbe–semiconductor hybrids against the H2-fed microbes.

Supplementary Data 5

LC-MS results of the metabolome in X. autotrophicus under different experimental conditions.

Supplementary Data 6

Fold changes of metabolites comparing the microbe–semiconductor hybrids against the H2-fed microbes.

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Guan, X., Erşan, S., Hu, X. et al. Maximizing light-driven CO2 and N2 fixation efficiency in quantum dot–bacteria hybrids. Nat Catal 5, 1019–1029 (2022). https://doi.org/10.1038/s41929-022-00867-3

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