Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Wastewater denitrification driven by mechanical energy through cellular piezo-sensitization

Nature Water volume 2, pages 531–540 (2024)Cite this article

Subjects

Abstract

Mechanical energy as a main energy form in wastewater treatment plants is generally used to enhance the physical mixing of reactor compartments. However, utilizing mechanical energy for directly driving microbial metabolism has not been explored. Here we developed an innovative mechano-driven bio-denitrification approach, whereby the electronic energy produced from mechanical energy by piezoelectric materials supported the metabolism of denitrifying microorganisms. When autotrophic denitrifying bacterium Thiobacillus denitrificans was stimulated with in situ formed struvite under mechanical agitation, a powerful cellular piezo-sensitization enabled nearly 100% nitrate reduction in synthetic wastewater with H2O as the electron donor. Such a self-sustained bio-denitrification process powered by mechanical energy was successfully implemented in real wastewater treatment, resulting in a maximum 117% increase of nitrate removal. These findings introduce a new paradigm for wastewater denitrification, unveiling previously unappreciated mechanisms for the energy–microbe–element nexus during wastewater treatment, and offer crucial insights for optimizing wastewater treatment plant operation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Schematic diagram of wastewater denitrification driven by mechanical energy.
Fig. 2: Design and characterization of the T. denitrificans-struvite biohybrids.
Fig. 3: Denitrification performance driven by mechanical agitation with T. denitrificans-struvite.
Fig. 4: Mechanisms of denitrification process driven by T. denitrificans-struvite under mechanical agitation.
Fig. 5: Wastewater denitrification driven by mechanical agitation.

Similar content being viewed by others

Data availability

The data supporting the findings of this study are available within the paper and its Supplementary Information.

References

  1. Lu, H., Chandran, K. & Stensel, D. Microbial ecology of denitrification in biological wastewater treatment. Water Res. 64, 237–254 (2014).

    Article  CAS  PubMed  Google Scholar 

  2. Dueholm, M. K. D. et al. MiDAS 4: a global catalogue of full-length 16S rRNA gene sequences and taxonomy for studies of bacterial communities in wastewater treatment plants. Nat. Commun. 13, 1908 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Zhang, S., Zheng, H. & Tratnyek, P. G. Advanced redox processes for sustainable water treatment. Nat. Water https://doi.org/10.1038/s44221-023-00098-1 (2023).

  4. Wunderlin, P. et al. Mechanisms of N2O production in biological wastewater treatment under nitrifying and denitrifying conditions. Water Res. 46, 1027–1037 (2012).

    Article  CAS  PubMed  Google Scholar 

  5. Ortmeyer, F. et al. Comparison of denitrification induced by various organic substances—reaction rates, microbiology, and temperature effect. Water Resour. Res. 57, e2021WR029793 (2021).

    Article  CAS  Google Scholar 

  6. Chen, F. et al. Coupled sulfur and electrode-driven autotrophic denitrification for significantly enhanced nitrate removal. Water Res. 220, 118675 (2022).

    Article  CAS  PubMed  Google Scholar 

  7. Hu, Y. et al. Iron sulphides mediated autotrophic denitrification: an emerging bioprocess for nitrate pollution mitigation and sustainable wastewater treatment. Water Res. 179, 115914 (2020).

    Article  CAS  PubMed  Google Scholar 

  8. Di Capua, F., Pirozzi, F., Lens, P. N. & Esposito, G. Electron donors for autotrophic denitrification. Chem. Eng. J. 362, 922–937 (2019).

    Article  Google Scholar 

  9. González-Cabaleiro, R., Ofiţeru, I. D., Lema, J. M. & Rodríguez, J. Microbial catabolic activities are naturally selected by metabolic energy harvest rate. ISME J. 9, 2630–2641 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Panepinto, D. et al. Evaluation of the energy efficiency of a large wastewater treatment plant in Italy. Appl. Energ. 161, 404–411 (2016).

    Article  CAS  Google Scholar 

  11. Rumbaugh, K. P. & Sauer, K. Biofilm dispersion. Nat. Rev. Microbiol. 18, 571–586 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Blume, T. & Neis, U. Improved wastewater disinfection by ultrasonic pre-treatment. Ultrason. Sonochem. 11, 333–336 (2004).

    Article  CAS  PubMed  Google Scholar 

  13. Naddeo, V., Landi, M., Belgiorno, V. & Napoli, R. Wastewater disinfection by combination of ultrasound and ultraviolet irradiation. J. Hazard. Mater. 168, 925–929 (2009).

    Article  CAS  PubMed  Google Scholar 

  14. Marino, A. A. & Becker, R. O. Piezoelectric effect and growth control in bone. Nature 228, 473–474 (1970).

    Article  CAS  PubMed  Google Scholar 

  15. Chen, M. et al. Mechanisms of nitrous oxide emission during photoelectrotrophic denitrification by self-photosensitized Thiobacillus denitrificans. Water Res. 172, 115501 (2020).

    Article  CAS  PubMed  Google Scholar 

  16. Hao, X., Wang, C., Van Loosdrecht, M. C. & Hu, Y. Looking beyond struvite for P-recovery. Environ. Sci. Technol. 47, 4965–4966 (2013).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  18. Banks, E., Chianelli, R. & Pintchovsky, F. The growth of some alkaline earth orthophosphates in gelatin gels. J. Cryst. Growth 18, 185–190 (1973).

    Article  CAS  Google Scholar 

  19. Prywer, J. et al. First experimental evidence of the piezoelectric nature of struvite. Sci Rep. 11, 14860 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Prywer, J. et al. First experimental evidences of the ferroelectric nature of struvite. Cryst. Growth Des. 20, 4454–4460 (2020).

    Article  CAS  Google Scholar 

  21. Nagarajan, V. et al. Realizing intrinsic piezoresponse in epitaxial submicron lead zirconate titanate capacitors on Si. Appl. Phys. Lett. 81, 4215–4217 (2002).

    Article  CAS  Google Scholar 

  22. Rouff, A. A. & Juarez, K. M. Zinc interaction with struvite during and after mineral formation. Environ. Sci. Technol. 48, 6342–6349 (2014).

    Article  CAS  PubMed  Google Scholar 

  23. Wei, L. et al. New insights into the adsorption behavior and mechanism of alginic acid onto struvite crystals. Chem. Eng. J. 358, 1074–1082 (2019).

    Article  CAS  Google Scholar 

  24. Luo, Y. et al. Bacterial mineralization of struvite using MgO as magnesium source and its potential for nutrient recovery. Chem. Eng. J. 351, 195–202 (2018).

    Article  CAS  Google Scholar 

  25. Rogée, L. et al. Ferroelectricity in untwisted heterobilayers of transition metal dichalcogenides. Science 376, 973–978 (2022).

    Article  PubMed  Google Scholar 

  26. Gruverman, A., Alexe, M. & Meier, D. Piezoresponse force microscopy and nanoferroic phenomena. Nat. Commun. 10, 1661 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Bowen, C., Kim, H., Weaver, P. & Dunn, S. Piezoelectric and ferroelectric materials and structures for energy harvesting applications. Energ. Environ. Sci. 7, 25–44 (2014).

    Article  CAS  Google Scholar 

  28. Thrash, J. C. & Coates, J. D. Direct and indirect electrical stimulation of microbial metabolism. Environ. Sci. Technol. 42, 3921–3931 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Jiang, T., Gao, C., Ma, C. & Xu, P. Microbial lactate utilization: enzymes, pathogenesis, and regulation. Trends Microbiol. 22, 589–599 (2014).

    Article  CAS  PubMed  Google Scholar 

  30. Aulenta, F. et al. Electron transfer from a solid-state electrode assisted by methyl viologen sustains efficient microbial reductive dechlorination of TCE. Environ. Sci. Technol. 41, 2554–2559 (2007).

    Article  CAS  PubMed  Google Scholar 

  31. Cheng, C. et al. Verifying the charge‐transfer mechanism in S‐scheme heterojunctions using femtosecond transient absorption spectroscopy. Angew. Chem. 135, e202218688 (2023).

    Article  Google Scholar 

  32. Zhou, X. et al. Mechanisms of extracellular photoelectron uptake by a Thiobacillus denitrificans-cadmium sulfide biosemiconductor system. Chem. Eng. J. 468, 143667 (2023).

    Article  CAS  Google Scholar 

  33. Fang, Y. et al. Microbial denitrification dominates nitrate losses from forest ecosystems. Proc. Natl Acad. Sci. USA 112, 1470–1474 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  35. Chen, M. et al. Light-driven nitrous oxide production via autotrophic denitrification by self-photosensitized Thiobacillus denitrificans. Environ. Int. 127, 353–360 (2019).

    Article  CAS  PubMed  Google Scholar 

  36. Wu, J. Understanding the electric double-layer structure, capacitance, and charging dynamics. Chem. Rev. 122, 10821–10859 (2022).

    Article  CAS  PubMed  Google Scholar 

  37. Matthies, D. et al. High-resolution structure and mechanism of an F/V-hybrid rotor ring in a Na+-coupled ATP synthase. Nat. Commun. 5, 5286 (2014).

    Article  PubMed  Google Scholar 

  38. Leone, V., Pogoryelov, D., Meier, T. & Faraldo-Gómez, J. D. On the principle of ion selectivity in Na+/H+-coupled membrane proteins: experimental and theoretical studies of an ATP synthase rotor. Proc. Natl Acad. Sci. USA 112, E1057–E1066 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Beller, H. R. et al. The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J. Bacteriol. 188, 1473–1488 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Lowe, E. C. et al. Quinol-cytochrome c oxidoreductase and cytochrome c4 mediate electron transfer during selenate respiration in Thauera selenatis. J. Biol. Chem. 285, 18433–18442 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Logan, B. E., Rossi, R., Ragab, A. A. & Saikaly, P. E. Electroactive microorganisms in bioelectrochemical systems. Nat. Rev. Microbiol. 17, 307–319 (2019).

    Article  CAS  PubMed  Google Scholar 

  42. Vidales, A. G., Bruant, G., Omanovic, S. & Tartakovsky, B. Carbon dioxide conversion to C1–C2 compounds in a microbial electrosynthesis cell with in situ electrodeposition of nickel and iron. Electrochim. Acta 383, 138349 (2021).

    Article  Google Scholar 

  43. Zhou, G.-W. et al. Mobile incubator for iron (III) reduction in the gut of the soil-feeding earthworm Pheretima guillelmi and interaction with denitrification. Environ. Sci. Technol. 53, 4215–4223 (2019).

    Article  CAS  PubMed  Google Scholar 

  44. Bhatnagar, L., Krzycki, J. & Zeikus, J. J. F. M. L. Analysis of hydrogen metabolism in Methanosarcina barkeri: regulation of hydrogenase and role of CO-dehydrogenase in H2 production. FEMS Microbiol. Lett. 41, 337–343 (1987).

    Article  CAS  Google Scholar 

  45. Liu, J. et al. Metal-free efficient photocatalyst for stable visible water splitting via a two-electron pathway. Science 347, 970–974 (2015).

    Article  CAS  PubMed  Google Scholar 

  46. Zheng, M. et al. Biochar as a carrier of struvite precipitation for nitrogen and phosphorus recovery from urine. J. Environ. Eng. 144, 04018101 (2018).

    Article  Google Scholar 

  47. Jiang, G., Gutierrez, O. & Yuan, Z. The strong biocidal effect of free nitrous acid on anaerobic sewer biofilms. Water Res. 45, 3735–3743 (2011).

    Article  CAS  PubMed  Google Scholar 

  48. Fessler, M., Madsen, J. S. & Zhang, Y. Microbial interactions in electroactive biofilms for environmental engineering applications: a role for nonexoelectrogens. Environ. Sci. Technol. 56, 15273–15279 (2022).

    Article  CAS  PubMed  Google Scholar 

  49. Guerin, S. et al. Control of piezoelectricity in amino acids by supramolecular packing. Nat. Mater. 17, 180–186 (2018).

    Article  CAS  PubMed  Google Scholar 

  50. Nguyen, V., Zhu, R., Jenkins, K. & Yang, R. J. N. C. Self-assembly of diphenylalanine peptide with controlled polarization for power generation. Nat. Commun. 7, 13566 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Fukada, E. & Yasuda, I. Piezoelectric effects in collagen. Jpn J. Appl. Phys. 3, 117 (1964).

    Article  CAS  Google Scholar 

  52. Yucel, T., Cebe, P. & Kaplan, D. L. Structural origins of silk piezoelectricity. Adv. Funct. Mater. 21, 779–785 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Ando, Y., Fukada, E. & Glimcher, M. J. Piezoelectricity of chitin in lobster shell and apodeme. Biorheology 14, 175–179 (1977).

    Article  CAS  PubMed  Google Scholar 

  54. Rajala, S. et al. Cellulose nanofibril film as a piezoelectric sensor material. ACS Appl. Mater. Interfaces 8, 15607–15614 (2016).

    Article  CAS  PubMed  Google Scholar 

  55. Ye, J. et al. Solar-driven methanogenesis with ultrahigh selectivity by turning down H2 production at biotic-abiotic interface. Nat. Commun. 13, 6612 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Hu, A. et al. Metal‐free semiconductor‐based bio‐nano hybrids for sustainable CH2‐to‐CH4 conversion with high quantum yield. Angew. Chem. 134, e202206508 (2022).

    Article  Google Scholar 

  57. Su, R. et al. Strain‐engineered nano‐ferroelectrics for high‐efficiency piezocatalytic overall water splitting. Angew. Chem. Int. Edit. 60, 16019–16026 (2021).

    Article  CAS  Google Scholar 

  58. Huang, S. et al. Sunlight significantly enhances soil denitrification via an interfacial biophotoelectrochemical pathway. Environ. Sci. Technol. 57, 7733–7742 (2023).

    Article  CAS  PubMed  Google Scholar 

  59. Ren, G. et al. Graphite-assisted electro-fermentation methanogenesis: spectroelectrochemical and microbial community analyses of cathode biofilms. Bioresource Technol. 269, 74–80 (2018).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The project was supported by the National Science Fund for Distinguished Young Scholars (41925028 to S.Z.), the National Science Fund for excellent Young Scholars (42322706 to J.Y.) and the National Natural Science Foundation of China (42307176 to G.R. and 42177206 to J.Y.).

Author information

Author notes

  1. These authors contributed equally: Jie Ye, Guoping Ren.

Authors and Affiliations

  1. Fujian Provincial Key Laboratory of Soil Environmental Health and Regulation, College of Resources and Environment, Fujian Agriculture and Forestry University, Fuzhou, China

    Jie Ye, Guoping Ren, Lu Liu, Dong Zhang, Raymond Jianxiong Zeng & Shungui Zhou

  2. Department of Biotechnology, Delft University of Technology, Delft, the Netherlands

    Mark C. M. van Loosdrecht

Authors
  1. Jie Ye
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guoping Ren
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raymond Jianxiong Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mark C. M. van Loosdrecht
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shungui Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.Y., G.R. and S.Z. conceived the idea for this work. G.R., J.Y., L.L. and D.Z. performed the characterizations, catalytic measurements, microbial community analyses and transcriptomic experiments. G.R., J.Y., L.L. and R.J.Z. analysed the data. J.Y., G.R., D.Z., R.J.Z., M.C.M.v.L. and S.Z. wrote the manuscript. R.J.Z., M.C.M.v.L. and S.Z. supervised the research.

Corresponding author

Correspondence to Shungui Zhou.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Water thanks the anonymous reviewers 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 text, Figs. 1–28 and Tables 1–5.

Supplementary Data 1

Source data for Supplementary Figs. 1–28.

Source data

Source Data Fig. 2

Source data for Fig. 2e,f.

Source Data Fig. 3

Source data for Fig. 3a–f.

Source Data Fig. 4

Source data for Fig. 3e.

Source Data Fig. 5

Source data for Fig. 5a–e.

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

Ye, J., Ren, G., Liu, L. et al. Wastewater denitrification driven by mechanical energy through cellular piezo-sensitization. Nat Water 2, 531–540 (2024). https://doi.org/10.1038/s44221-024-00253-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s44221-024-00253-2

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing