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A soil-inspired dynamically responsive chemical system for microbial modulation

Nature Chemistry volume 15, pages 119–128 (2023)Cite this article

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Abstract

Interactions between the microbiota and their colonized environments mediate critical pathways from biogeochemical cycles to homeostasis in human health. Here we report a soil-inspired chemical system that consists of nanostructured minerals, starch granules and liquid metals. Fabricated via a bottom-up synthesis, the soil-inspired chemical system can enable chemical redistribution and modulation of microbial communities. We characterize the composite, confirming its structural similarity to the soil, with three-dimensional X-ray fluorescence and ptychographic tomography and electron microscopy imaging. We also demonstrate that post-synthetic modifications formed by laser irradiation led to chemical heterogeneities from the atomic to the macroscopic level. The soil-inspired material possesses chemical, optical and mechanical responsiveness to yield write–erase functions in electrical performance. The composite can also enhance microbial culture/biofilm growth and biofuel production in vitro. Finally, we show that the soil-inspired system enriches gut bacteria diversity, rectifies tetracycline-induced gut microbiome dysbiosis and ameliorates dextran sulfate sodium-induced rodent colitis symptoms within in vivo rodent models.

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Fig. 1: Soil-inspired dynamically responsive chemical system for microbial modulation.
Fig. 2: X-ray ptychographic, fluorescence tomography and in situ IR spectra reveal chemical composition and dynamics.
Fig. 3: Soil-inspired material with tunable conductivity under mechanical and chemical stimuli.
Fig. 4: Laser-assisted chemical modification for biofilm growth enhancement.
Fig. 5: Soil-inspired material for gut microbiome modulation and DSS-induced colitis therapy in vivo.

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Data availability

All data supporting the findings of this study are available within the Article, its Supplementary Information and Supplementary Files. Data are also available from the corresponding authors upon reasonable request. Source data are available at https://osf.io/muc9g/?view_only=971b8fde8562427ab619bc30c2624cb7. Source data are provided with this Paper.

Code availability

For PtychoShelves, code is available at https://www.psi.ch/en/sls/csaxs/software, and for PtychoLib, at https://github.com/kyuepublic/ptychopy.

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Acknowledgements

We thank Dr. K. Watters for the scientific editing of the manuscript. This work was supported by the US Office of Naval Research (N000141612958), the National Science Foundation (NSF CMMI-1848613) and a Zhong Ziyi Educational Foundation Award. This work was partially supported by the University of Chicago Materials Research Science and Engineering Center, which is funded by the National Science Foundation under award no. DMR-2011854. This work used instruments in the Electron Microscopy Service (Research Resources Center, UIC). This work made use of the BioCryo facility of Northwestern University’s NUANCE Center, which has received support from the SHyNE Resource (NSF ECCS-2025633), the IIN and Northwestern’s MRSEC programme (NSF DMR-1720139). Use of the Advanced Photon Source and the Center for Nanoscale Materials, both US Department of Energy Office of Science User Facilities, was supported by the US Department of Energy, Office of Science, under contract no. DE-AC02-06CH11357. The BNP was obtained through an NIH ARRA S10 grant no. SP0007167, and S.C. also acknowledges the support of DOE grant no. PRJ1009594. We also thank Dr. A. Tokmakoff and Dr. Z. Lu for their support and helpful discussions.

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Author notes

  1. These authors contributed equally: Yiliang Lin, Xiang Gao, Jiping Yue, Yin Fang.

Authors and Affiliations

  1. The James Franck Institute, University of Chicago, Chicago, IL, USA

    Yiliang Lin, Xiang Gao, Yin Fang, Xin-Xing Zhang, Aleksander Prominski & Bozhi Tian

  2. Department of Chemistry, University of Chicago, Chicago, IL, USA

    Jiping Yue, Jiuyun Shi, Clementene Clayton, Xin-Xing Zhang, Aleksander Prominski & Bozhi Tian

  3. Pritzker School of Molecular Engineering, University of Chicago, Chicago, IL, USA

    Lingyuan Meng & Philip Griffin

  4. The Institute for Biophysical Dynamics, University of Chicago, Chicago, IL, USA

    Xin-Xing Zhang, Aleksander Prominski & Bozhi Tian

  5. Electron Microscopy Core, Research Resources Center, University of Illinois Chicago, Chicago, IL, USA

    Fengyuan Shi

  6. Advanced Photon Source, Argonne National Laboratory, Lemont, IL, USA

    Junjing Deng, Si Chen, Yi Jiang, Fabricio Marin & Zhonghou Cai

  7. Department of Chemistry, Northwestern University, Evanston, IL, USA

    Jingtian Hu & Teri W. Odom

  8. Department of Radiology, University of Chicago, Chicago, IL, USA

    Hsiu-Ming Tsai

  9. Department of Materials Science and Engineering, Northwestern University, Evanston, IL, USA

    Qing Tu, Reiner Bleher & Teri W. Odom

  10. NUANCE Center, Northwestern University, Evanston, IL, USA

    Eric W. Roth, Reiner Bleher & Xinqi Chen

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  1. Yiliang Lin
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Contributions

B.T. supervised the research. Y.L. and B.T. conceived the idea. Y.L., X.G., J.Y. and B.T. developed the methods. Y.L., X.G., J.Y., Y.F., J.S., L.M., C.C., X.-X.Z., H.-M.T., F.S., J.H., Q.T., E.W.R., R.B., X.C., P.G., Z.C., J.D., S.C. and A.P. performed the experiments. Y.J., J.Y., H.-M.T. and F.M. analysed and processed the data. Y.L., X.G., J.Y. and B.T. wrote the paper, with comments from all authors.

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Correspondence to Yiliang Lin or Bozhi Tian.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–51 and Tables 1 and 2.

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Supplementary Video 1

Focused ion beam tomography images of soil-inspired material showing the soil-inspired material is porous, which is consistent with X-ray ptychography and fluorescence imaging, and cross-sectional TEM images.

Source data

Source Data Fig. 2

FTIR spectra.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 4

Statistical source data.

Source Data Fig. 5

Statistical source data.

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Lin, Y., Gao, X., Yue, J. et al. A soil-inspired dynamically responsive chemical system for microbial modulation. Nat. Chem. 15, 119–128 (2023). https://doi.org/10.1038/s41557-022-01064-2

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