Skip to main content

Advertisement

Log in

Solar-driven waste-to-chemical conversion by wastewater-derived semiconductor biohybrids

  • Article
  • Published:

From Nature Sustainability

View current issue Submit your manuscript

Abstract

Semiconductor biohybrids integrating the merits of living cells and semiconductor materials have the potential to shift the current energy-intensive chemical production system to a more sustainable one by offering efficient solar-to-chemical conversion. However, cost-competitive and environmentally friendly scaling-up approaches are still urgently needed. To tackle this challenge, we propose a strategy that co-utilizes pollutants in wastewater to produce semiconductor biohybrids in-situ for scalable solar-to-chemical conversion. Specifically, we introduce an aerobic sulfate reduction pathway into Vibrio natriegens to enable the direct utilization of heavy metal ions (that is, Cd2+), sulfate and organics in wastewater to biosynthesize functional semiconductor nanoparticles in living V. natriegens to assemble semiconductor biohybrids. Meanwhile, a designated biosynthetic pathway is introduced into the biohybrids to enable the production of 2,3-butanediol, a valuable bulk chemical with wide applications, from organics in wastewater. Using the obtained biohybrids, the production of 2,3-butanediol reaches 13.09 g l−1 in a 5-l illuminated fermenter using wastewater as the feedstock, revealing its scalability. Life-cycle assessment shows that this specific biohybrid route has substantial sustainability gain compared with conventional 2,3-butanediol production routes. This work can bring solar-driven biomanufacturing and waste-to-wealth conversion one step forward and pave the way to cleaner production and circular economy.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1: Schematic of solar-driven chemical production by semiconductor biohybrids synthesized from wastewater pollutants using engineered V. natriegens.
Fig. 2: Designing V. natriegens to produce semiconductor biohybrids from wastewater.
Fig. 3: Solar-to-chemical production by the semiconductor biohybrids from wastewater.
Fig. 4: Scaling up of chemical production with biohybrid system using real wastewater.
Fig. 5: Life-cycle assessment.

Similar content being viewed by others

Data availability

All data presented in this manuscript are available in the paper and its Supplementary Information. Figures 15 and Supplementary Figs. 114, 16, 18 and 20 are available on Figshare at https://doi.org/10.6084/m9.figshare.24115851. Source data are provided with this paper.

References

  1. Scown, C. D. & Keasling, J. D. Sustainable manufacturing with synthetic biology. Nat. Biotechnol. 40, 304–307 (2022).

    CAS  Google Scholar 

  2. Liew, F. E. et al. Carbon-negative production of acetone and isopropanol by gas fermentation at industrial pilot scale. Nat. Biotechnol. 40, 335–344 (2022).

    CAS  Google Scholar 

  3. Liu, Y. Z. et al. Biofuels for a sustainable future. Cell 184, 1636–1647 (2021).

    CAS  Google Scholar 

  4. Jones, S. W. et al. CO2 fixation by anaerobic non-photosynthetic mixotrophy for improved carbon conversion. Nat. Commun. 7, 12800 (2016).

    CAS  Google Scholar 

  5. Sakimoto, K. K., Wong, A. B. & Yang, P. D. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science 351, 74–77 (2016).

    CAS  Google Scholar 

  6. Guo, J. L. et al. Light-driven fine chemical production in yeast biohybrids. Science 362, 813–816 (2018).

    CAS  Google Scholar 

  7. Cestellos-Blanco, S., Zhang, H., Kim, J. M., Shen, Y. X. & Yang, P. D. Photosynthetic semiconductor biohybrids for solar-driven biocatalysis. Nat. Catal. 3, 245–255 (2020).

    CAS  Google Scholar 

  8. Kornienko, N., Zhang, J. Z., Sakimoto, K. K., Yang, P. D. & Reisner, E. Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis. Nat. Nanotechnol. 13, 890–899 (2018).

    CAS  Google Scholar 

  9. Cestellos-Blanco, S., Kim, J. M., Watanabe, N. G., Chan, R. R. & Yang, P. D. Molecular insights and future frontiers in cell photosensitization for solar-driven CO2 conversion. iScience 24, 102952 (2021).

    CAS  Google Scholar 

  10. Kang, S. H., Bozhilov, K. N., Myung, N. V., Mulchandani, A. & Chen, W. Microbial synthesis of CdS nanocrystals in genetically engineered E. coli. Angew. Chem. Int. Ed. 47, 5186–5189 (2008).

    CAS  Google Scholar 

  11. Kornienko, N. et al. Spectroscopic elucidation of energy transfer in hybrid inorganic-biological organisms for solar-to-chemical production. Proc. Natl Acad. Sci. USA 113, 11750–11755 (2016).

    CAS  Google Scholar 

  12. Wang, B., Jiang, Z. F., Yu, J. C., Wang, J. F. & Wong, P. K. Enhanced CO2 reduction and valuable C2+ chemical production by a CdS-photosynthetic hybrid system. Nanoscale 11, 9296–9301 (2019).

    CAS  Google Scholar 

  13. Yan, N., Zhou, K., Tong, Y. W., Leong, D. T. & Dickieson, M. P. Pathways to food from CO2 via ‘green chemical farming’. Nat. Sustain. 5, 907–909 (2022).

    Google Scholar 

  14. Li, W. W., Yu, H. Q. & Rittmann, B. E. Chemistry: reuse water pollutants. Nature 528, 29–31 (2015).

    CAS  Google Scholar 

  15. Sullivan, K. P. et al. Mixed plastics waste valorization through tandem chemical oxidation and biological funneling. Science 378, 207–211 (2022).

    CAS  Google Scholar 

  16. Atelge, M. R. et al. Biogas production from organic waste: recent progress and perspectives. Waste Biomass Valor. 11, 1019–1040 (2020).

    CAS  Google Scholar 

  17. Sun, G. L., Reynolds, E. E. & Belcher, A. M. Using yeast to sustainably remediate and extract heavy metals from waste waters. Nat. Sustain. 3, 303–311 (2020).

    Google Scholar 

  18. Oh, S. & Logan, B. E. Hydrogen and electricity production from a food processing wastewater using fermentation and microbial fuel cell technologies. Water Res. 39, 4673–4682 (2005).

    CAS  Google Scholar 

  19. Nam, J. Y., Yates, M. D., Zaybak, Z. & Logan, B. E. Examination of protein degradation in continuous flow, microbial electrolysis cells treating fermentation wastewater. Bioresour. Technol. 171, 182–186 (2014).

    CAS  Google Scholar 

  20. Kieu, H. T., Muller, E. & Horn, H. Heavy metal removal in anaerobic semi-continuous stirred tank reactors by a consortium of sulfate-reducing bacteria. Water Res. 45, 3863–3870 (2011).

    CAS  Google Scholar 

  21. Javanbakht, V., Alavi, S. A. & Zilouei, H. Mechanisms of heavy metal removal using microorganisms as biosorbent. Water Sci. Technol. 69, 1775–1787 (2014).

    CAS  Google Scholar 

  22. De Vrieze, J., Coma, M., Debeuckelaere, M., Van der Meeren, P. & Rabaey, K. High salinity in molasses wastewaters shifts anaerobic digestion to carboxylate production. Water Res. 98, 293–301 (2016).

    Google Scholar 

  23. Jassby, D., Cath, T. Y. & Buisson, H. The role of nanotechnology in industrial water treatment. Nat. Nanotechnol. 13, 670–672 (2018).

    CAS  Google Scholar 

  24. Wang, C. L., Maratukulam, P. D., Lum, A. M., Clark, D. S. & Keasling, J. D. Metabolic engineering of an aerobic sulfate reduction pathway and its application to precipitation of cadmium on the cell surface. Appl. Environ. Microbiol. 66, 4497–4502 (2000).

    CAS  Google Scholar 

  25. Zeng, Q., Hao, T. W., Mackey, H. R., van Loosdrecht, M. C. M. & Chen, G. H. Recent advances in dissimilatory sulfate reduction: from metabolic study to application. Water Res. 150, 162–181 (2019).

    Google Scholar 

  26. Xu, J. Q., Yang, S. & Yang, L. R. Vibrio natriegens as a host for rapid biotechnology. Trends Biotechnol. 40, 381–384 (2022).

    CAS  Google Scholar 

  27. Tait, S., Clarke, W. P., Keller, J. & Batstone, D. J. Removal of sulfate from high-strength wastewater by crystallisation. Water Res. 43, 762–772 (2009).

    CAS  Google Scholar 

  28. Riahi, S. & Rowley, C. N. Why can hydrogen sulfide permeate cell membranes? J. Am. Chem. Soc. 136, 15111–15113 (2014).

    CAS  Google Scholar 

  29. Sakpirom, J., Kantachote, D., Siripattanakul-Ratpukdi, S., McEvoy, J. & Khan, E. Simultaneous bioprecipitation of cadmium to cadmium sulfide nanoparticles and nitrogen fixation by Rhodopseudomonas palustris TN110. Chemosphere 223, 455–464 (2019).

    CAS  Google Scholar 

  30. Wang, B. et al. Biohybrid photoheterotrophic metabolism for significant enhancement of biological nitrogen fixation in pure microbial cultures. Energy Environ. Sci. 12, 2185–2191 (2019).

    CAS  Google Scholar 

  31. Xu, R. et al. New double network hydrogel adsorbent: highly efficient removal of Cd(II) and Mn(II) ions in aqueous solution. Chem. Eng. J. 275, 179–188 (2015).

    CAS  Google Scholar 

  32. Luo, X. B., Xi, Y., Yu, H. Y., Yin, X. C. & Luo, S. L. Capturing cadmium(II) ion from wastewater containing solid particles and floccules using ion-imprinted polymers with broom effect. Ind. Eng. Chem. Res. 56, 2350–2358 (2017).

    CAS  Google Scholar 

  33. Liu, T. Y., Yang, X., Wang, Z. L. & Yan, X. X. Enhanced chitosan beads-supported Fe0-nanoparticles for removal of heavy metals from electroplating wastewater in permeable reactive barriers. Water Res. 47, 6691–6700 (2013).

    CAS  Google Scholar 

  34. Suzuki, Y., Kametani, T. & Maruyama, T. Removal of heavy metals from aqueous solution by nonliving Ulva seaweed as biosorbent. Water Res. 39, 1803–1808 (2005).

    CAS  Google Scholar 

  35. Goncalves, M. M. M., da Costa, A. C. A., Leite, S. G. F. & Sant′Anna, G. L. Jr Heavy metal removal from synthetic wastewaters in an anaerobic bioreactor using stillage from ethanol distilleries as a carbon source. Chemosphere 69, 1815–1820 (2007).

    CAS  Google Scholar 

  36. D’Angelo, S. C., Dall’Ara, A., Mondelli, C., Pérez-Ramírez, J. & Papadokonstantakis, S. Techno-economic analysis of a glycerol biorefinery. ACS Sustain. Chem. Eng. 6, 16563–16572 (2018).

    Google Scholar 

  37. Quispe, C. A. G., Coronado, C. J. R. & Carvalho, J. A. Jr. Glycerol: production, consumption, prices, characterization and new trends in combustion. Renew. Sustain. Energy Rev. 27, 475–493 (2013).

    CAS  Google Scholar 

  38. Ye, J. et al. Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri-CdS biohybrid. Appl. Catal. B 257, 117916 (2019).

    CAS  Google Scholar 

  39. Ji, X. J., Huang, H. & Ouyang, P. K. Microbial 2,3-butanediol production: a state-of-the-art review. Biotechnol. Adv. 29, 351–364 (2011).

    CAS  Google Scholar 

  40. Celinska, E. & Grajek, W. Biotechnological production of 2,3-butanediol-current state and prospects. Biotechnol. Adv. 27, 715–725 (2009).

    CAS  Google Scholar 

  41. Xu, Y. Q. et al. Systematic metabolic engineering of Escherichia coli for high-yield production of fuel bio-chemical 2,3-butanediol. Metab. Eng. 23, 22–33 (2014).

    CAS  Google Scholar 

  42. Zhang, H. et al. Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production. Nat. Nanotechnol. 13, 900–905 (2018).

    CAS  Google Scholar 

  43. Wei, W. et al. A surface-display biohybrid approach to light-driven hydrogen production in air. Sci. Adv. 4, eaap9253 (2018).

    Google Scholar 

  44. Ding, Y. C. et al. Nanorg microbial factories: light-driven renewable biochemical synthesis using quantum dot-bacteria nanobiohybrids. J. Am. Chem. Soc. 141, 10272–10282 (2019).

    CAS  Google Scholar 

  45. Wang, M., Chen, B. Q., Fang, Y. M. & Tan, T. W. Cofactor engineering for more efficient production of chemicals and biofuels. Biotechnol. Adv. 35, 1032–1039 (2017).

    CAS  Google Scholar 

  46. Zhang, R. T. et al. Proteomic and metabolic elucidation of solar-powered biomanufacturing by bio-abiotic hybrid system. Chem 6, 234–249 (2020).

    CAS  Google Scholar 

  47. Bo, T. T. et al. Photocatalytic H2 evolution on CdS modified with partially crystallized MoS2 under visible light irradiation. Chem. Phys. Lett. 746, 137305 (2020).

    CAS  Google Scholar 

  48. Jin, S. et al. Acetogenic bacteria utilize light-driven electrons as an energy source for autotrophic growth. Proc. Natl. Acad. Sci. USA 118, e2020552118 (2021).

    CAS  Google Scholar 

  49. Guan, X. et al. Maximizing light-driven CO2 and N2 fixation efficiency in quantum dot-bacteria hybrids. Nat. Catal. 5, 1019–1029 (2022).

    CAS  Google Scholar 

  50. Hu, W. Q., Tian, J. P., Zang, N., Gao, Y. & Chen, L. J. Study of the development and performance of centralized wastewater treatment plants in Chinese industrial parks. J. Clean. Prod. 214, 939–951 (2019).

    Google Scholar 

  51. Weinstock, M. T., Hesek, E. D., Wilson, C. M. & Gibson, D. G. Vibrio natriegens as a fast-growing host for molecular biology. Nat. Methods 13, 849–851 (2016).

    CAS  Google Scholar 

  52. Zhang, Y. et al. Systems metabolic engineering of Vibrio natriegens for the production of 1,3-propanediol. Metab. Eng. 65, 52–65 (2021).

    CAS  Google Scholar 

  53. Gao, X. et al. Engineering the methylerythritol phosphate pathway in cyanobacteria for photosynthetic isoprene production from CO2. Energy Environ. Sci. 9, 1400–1411 (2016).

    CAS  Google Scholar 

  54. Wernet, G. et al. The ecoinvent database version 3 (part I): overview and methodology. Int. J. Life Cycle Assess. 21, 1218–1230 (2016).

    Google Scholar 

  55. Lifecycle Analysis of Greenhouse Gas Emissions Under the Renewable Fuel Standard (US EPA, 2021).

  56. Dunn, J. B. et al. Life-cycle Analysis of Bioproducts and their Conventional Counterparts in GREET Technical Report (US Department of Energy, 2015).

  57. 2019 Refinement to the 2006 IPCC Guidelines for National Greenhouse Gas Inventories (IPCC, 2019).

  58. Jiang, H., Jin, Q., Cheng, P. P., Hua, M. & Ye, Z. How are typical urban sewage treatment technologies going in China: from the perspective of life cycle environmental and economic coupled assessment. Environ. Sci. Pollut. Res. 28, 45109–45120 (2021).

    CAS  Google Scholar 

  59. Pi, S. S. et al. Solar-driven waste-to-chemical conversion by wastewater-derived semiconductor biohybrids. Figshare https://doi.org/10.6084/m9.figshare.24115851 (2023).

Download references

Acknowledgements

We thank C. Zhong for valuable suggestions and discussion of this work and the Shenzhen Infrastructure for Synthetic Biology for instrument support and technical assistance. This work was supported by the National Natural Science Foundation of China (Grant No. 32230060, C.Y. and X.G.; Grant No. 22176046, L.L.; Grant No. 32171426, X.G.; Grant No. 52200090, S.P.), Shenzhen Science and Technology Program (Grant No. GXWD20220811173949005, KQTD20190929172630447 and JCYJ20210324124209025, L.L.; Grant No. JCYJ20220818101804010, RCYX20221008092901004, X.G.), the National Key R&D Program of China (Grant No. 2021YFA0910800, X.G.), State Key Laboratory of Urban Water Resource and Environment (Harbin Institute of Technology) (Grant No. 2021TS13, L.L.) and the Natural Science Foundation of Guangdong Province (Grant No. 2022A1515012016, L.L.).

Author information

Authors and Affiliations

Authors

Contributions

X.G., L.L., Y.L. and C.Y. supervised the research; X.G. and L.L. designed the experiments; S.P., W.Y. and W.F. contributed to the biohybrid production, and the structural and chemical characterizations; W. Cheng and S.P. performed the metabolic experiment, with the results verified by X.G.; S.P., R.Y. and W.Y. contributed to the wastewater-relevant experiments and fermenter data; L.C., Z.L., R.Y. and W. Chao performed the photoelectrochemical analysis; W. Chao, N.R., X.G. and L.L. contributed to the LCA data; S.P., X.G., Y.L., L.L., W.Y. and W. Chao wrote the manuscript and received comments from all the other authors.

Corresponding authors

Correspondence to Lu Lu or Xiang Gao.

Ethics declarations

Competing interests

L.L., X.G., R.Y., S.P. and W.Y. are co-inventors on filed China patents CN202310145122.9 and CN202210318999.9 related to the production of semiconductor nanoparticles and biohybrids directly from wastewater by engineered strains that incorporate discoveries included in this manuscript. The remaining authors declare no competing interests.

Peer review

Peer review information

Nature Sustainability thanks Shu Wang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, LCA, Tables 1–15, Figs. 1–21 and References.

Reporting Summary

Supplementary Data 1

Source data for Supplementary Figs. 1–14, 16, 18 and 20.

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data, EDS mapping data and photoelectrochemical data.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 4

Fermenter data.

Source Data Fig. 5

Statistical source data.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pi, S., Yang, W., Feng, W. et al. Solar-driven waste-to-chemical conversion by wastewater-derived semiconductor biohybrids. Nat Sustain 6, 1673–1684 (2023). https://doi.org/10.1038/s41893-023-01233-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41893-023-01233-2

  • Springer Nature Limited

This article is cited by

Navigation