Skip to main content
SpringerLink
Log in

Bioelectronic protein nanowire sensors for ammonia detection

  • Research Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

Electronic sensors based on biomaterials can lead to novel green technologies that are low cost, renewable, and eco-friendly. Here we demonstrate bioelectronic ammonia sensors made from protein nanowires harvested from the microorganism Geobacter sulfurreducens. The nanowire sensor responds to a broad range of ammonia concentrations (10 to 106 ppb), which covers the range relevant for industrial, environmental, and biomedical applications. The sensor also demonstrates high selectivity to ammonia compared to moisture and other common gases found in human breath. These results provide a proof-of-concept demonstration for developing protein nanowire based gas sensors for applications in industry, agriculture, environmental monitoring, and healthcare.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Kwak, D.; Lei, Y.; Maric, R. Ammonia gas sensors: A comprehensive review. Talanta2019, 204, 713–720.

    Article  CAS  Google Scholar 

  2. Ritz, C. W.; Fairchild, B. D.; Lacy, M. P. Implications of ammonia production and emissions from commercial poultry facilities: A review. J. Appl. Poult. Res.2004, 13, 684–692.

    Article  Google Scholar 

  3. van der Eerden, L. J. M.; de Visser, P. H. B.; van Dijk, C. J. Risk of damage to crops in the direct neighbourhood of ammonia sources. Environ. Pollut.1998, 102, 49–53.

    Article  CAS  Google Scholar 

  4. Rigoni, F.; Tognolini, S.; Borghetti, P.; Drera, G.; Pagliara, S.; Goldoni, A.; Sangaletti, L. Environmental monitoring of low-ppb ammonia concentrations based on single-wall carbon nanotube chemiresistor gas sensors: Detection limits, response dynamics, and moisture effects. Procedia Eng.2014, 87, 716–719.

    Article  CAS  Google Scholar 

  5. Baek, B. H.; Aneja, V. P.; Tong, Q. S. Chemical coupling between ammonia, acid gases, and fine particles. Environ. Pollut.2004, 129, 89–98.

    Article  CAS  Google Scholar 

  6. Kharitonov, S. A.; Barnes, P. J. Biomarkers of some pulmonary diseases in exhaled breath. Biomarkers2002, 7, 1–32.

    Article  CAS  Google Scholar 

  7. Bayrakli, I.; Turkmen, A.; Akman, H.; Sezer, M. T.; Kutluhan, S. Applications of external cavity diode laser-based technique to noninvasive clinical diagnosis using expired breath ammonia analysis: Chronic kidney disease, epilepsy. J. Biomed. Opt.2016, 21, 87004.

    Article  Google Scholar 

  8. Davies, S.; Spanel, P.; Smith, D. Quantitative analysis of ammonia on the breath of patients in end-stage renal failure. Kidney Int.1997, 52, 223–228.

    Article  CAS  Google Scholar 

  9. Hibbard, T.; Killard, A. J. Breath ammonia levels in a normal human population study as determined by photoacoustic laser spectroscopy. J. Breath Res.2011, 5, 037101.

    Article  CAS  Google Scholar 

  10. Bevc, S.; Mohorko, E.; Kolar, M.; Brglez, P.; Holobar, A.; Kniepeiss, D.; Podbregar, M.; Piko, N.; Hojs, N.; Knehtl, M. et al. Measurement of breath ammonia for detection of patients with chronic kidney disease. Clin. Nephrol.2017, 88, 14–17.

    Article  Google Scholar 

  11. Turner, C.; Španěl, P.; Smith, D. A longitudinal study of ammonia, acetone and propanol in the exhaled breath of 30 subjects using selected ion flow tube mass spectrometry, SIFT-MS. Physiol. Meas.2006, 27, 321–337.

    Article  Google Scholar 

  12. Mathew, T. L.; Pownraj, P.; Abdulla, S.; Pullithadathil, B. Technologies for clinical diagnosis using expired human breath analysis. Diagnostics2015, 5, 27–60.

    Article  CAS  Google Scholar 

  13. Güntner, A. T.; Righettoni, M.; Pratsinis, S. E. Selective sensing of NH3 by Si-doped-MoO3 for breath analysis. Sens. Actuators B: Chem.2016, 223, 266–273.

    Article  CAS  Google Scholar 

  14. Obermeier, J.; Trefz, P.; Happ, J.; Schubert, J. K.; Staude, H.; Fischer, D. C.; Miekisch, W. Exhaled volatile substances mirror clinical conditions in pediatric chronic kidney disease. PLoS One2017, 12, e0178745.

    Article  CAS  Google Scholar 

  15. Sawicka, K.; Gouma, P.; Simon, S. Electrospun biocomposite nanofibers for urea biosensing. Sens. Actuators B: Chem.2005, 108, 585–588.

    Article  CAS  Google Scholar 

  16. Narasimhan, L. R.; Goodman, W.; Patel, C. K. N. Correlation of breath ammonia with blood urea nitrogen and creatinine during hemodialysis. Proc. Natl. Acad. Sci. USA2001, 98, 4617–4621.

    Article  CAS  Google Scholar 

  17. Amano, A.; Yoshida, Y.; Oho, T.; Koga, T. Monitoring ammonia to assess halitosis. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod.2002, 94, 692–696.

    Article  Google Scholar 

  18. Turner, A. P. F. Biosensors: Sense and sensibility. Chem. Soc. Rev2013, 42, 3184–3196.

    Article  CAS  Google Scholar 

  19. Piloto, C.; Mirri, F.; Bengio, E. A.; Notarianni, M.; Gupta, B.; Shafiei, M.; Pasquali, M.; Motta, N. Room temperature gas sensing properties of ultrathin carbon nanotube films by surfactant-free dip coating. Sens. Actuators B: Chem.2016, 227, 128–134.

    Article  CAS  Google Scholar 

  20. Bekyarova, E.; Davis, M.; Burch, T.; Itkis, M. E.; Zhao, B.; Sunshine, S.; Haddon, R. C. Chemically functionalized single-walled carbon nanotubes as ammonia sensors. J. Phys. Chem. B.2004, 108, 19717–19720.

    Article  CAS  Google Scholar 

  21. Chopra, S.; Pham, A.; Gaillard, J.; Parker, A.; Rao, A. M. Carbonnanotube-based resonant-circuit sensor for ammonia. Appl. Phys. Lett.2002, 80, 4632–4634.

    Article  CAS  Google Scholar 

  22. Quang, N. H.; Van Trinh, M.; Lee, B. H.; Huh, J. S. Effect of NH3 gas on the electrical properties of single-walled carbon nanotube bundles. Sens. Actuators B: Chem.2006, 113, 341–346.

    Article  CAS  Google Scholar 

  23. Van Hieu, N.; Dung, N. Q.; Tam, P. D.; Trung, T.; Chien, N. D. Thin film polypyrrole/SWCNTs nanocomposites-based NH3 sensor operated at room temperature. Sens. Actuators B: Chem.2009, 140, 500–507.

    Article  CAS  Google Scholar 

  24. Duc Hoa, N.; Van Quy, N.; Suk Cho, Y.; Kim, D. Nanocomposite of SWNTs and SnO2 fabricated by soldering process for ammonia gas sensor application. Phys. Status Solidi2007, 204, 1820–1824.

    Article  CAS  Google Scholar 

  25. Rigoni, F.; Freddi, S.; Pagliara, S.; Drera, G.; Sangaletti, L.; Suisse, J. M.; Bouvet, M.; Malovichko, A. M.; Emelianov, A. V.; Bobrinetskiy, I. I. Humidity-enhanced sub-ppm sensitivity to ammonia of covalently functionalized single-wall carbon nanotube bundle layers. Nnanotechnology2017, 28, 255502.

    Article  CAS  Google Scholar 

  26. Fobelets, K.; Panteli, C.; Sydoruk, O.; Li, C. B. Ammonia sensing using arrays of silicon nanowires and graphene. J. Semicond.2018, 39, 063001.

    Article  CAS  Google Scholar 

  27. In, H. J.; Field, C. R.; Pehrsson, P. E. Periodically porous top electrodes on vertical nanowire arrays for highly sensitive gas detection. Nanotechnology2011, 22, 355501.

    Article  CAS  Google Scholar 

  28. Yang, L.; Lin, H. Y.; Zhang, Z. S.; Cheng, L.; Ye, S. Y.; Shao, M. W. Gas sensing of tellurium-modified silicon nanowires to ammonia and propylamine. Sens. Actuators B: Chem.2013, 177, 260–264.

    Article  CAS  Google Scholar 

  29. Schmädicke, C. Silicon nanowire based sensor for highly sensitive and selective detection of ammonia. Ph.D. Dissertation, The Technische Universität Dresden, Dresden, Germany, 2015.

    Google Scholar 

  30. Betty, C. A.; Choudhury, S.; Girija, K. G. Discerning specific gas sensing at room temperature by ultrathin SnO2 films using impedance approach. Sens. Actuators B: Chem.2012, 173, 781–788.

    Article  CAS  Google Scholar 

  31. Van Hieu, N.; Thuy, L. T. B.; Chien, N. D. Highly sensitive thin film NH3 gas sensor operating at room temperature based on SnO2/MWCNTs composite. Sens. Actuators B: Chem.2008, 129, 888–895.

    Article  CAS  Google Scholar 

  32. Kumar, L.; Rawal, I.; Kaur, A.; Annapoorni, S. Flexible room temperature ammonia sensor based on polyaniline. Sens. Actuators B: Chem.2017, 240, 408–416.

    Article  CAS  Google Scholar 

  33. Van Tuan, C.; Tuan, M. A.; Van Hieu, N.; Trung, T. Electrochemical synthesis of polyaniline nanowires on Pt interdigitated microelectrode for room temperature NH3 gas sensor application. Curr. Appl. Phys.2012, 12, 1011–1016.

    Article  Google Scholar 

  34. Deshpande, N. G.; Gudage, Y. G; Sharma, R.; Vyas, J. C.; Kim, J. B.; Lee, Y. P. Studies on tin oxide-intercalated polyaniline nanocomposite for ammonia gas sensing applications. Sens. Actuators B: Chem.2009, 138, 76–84.

    Article  CAS  Google Scholar 

  35. Tran, Q. T.; Hoa, H. T. M.; Yoo, D. H.; Cuong, T. V.; Hur, S. H.; Chung, J. S.; Kim, E. J.; Klohl, P. A. Reduced graphene oxide as an over-coating layer on silver nanostructures for detecting NH3 gas at room temperature. Sens. Actuators B: Chem.2014, 194, 45–50.

    Article  CAS  Google Scholar 

  36. Biskupski, D.; Herbig, B.; Schottner, G.; Moos, R. Nanosized titania derived from a novel sol-gel process for ammonia gas sensor applications. Sens. Actuators B: Chem.2011, 153, 329–334.

    Article  CAS  Google Scholar 

  37. Andre, R. S.; Kwak, D.; Dong, Q. C.; Zhong, W.; Correa, D. S.; Mattoso, L. H. C.; Lei, Y. Sensitive and selective NH3 monitoring at room temperature using ZnO ceramic nanofibers decorated with poly(styrene sulfonate). Sensors (Basel)2018, 18, 1058.

    Article  CAS  Google Scholar 

  38. Pang, Z. Y.; Yang, Z. P.; Chen, Y.; Zhang, J. N.; Wang, Q. Q.; Huang, F. L.; Wei, Q. F. A room temperature ammonia gas sensor based on cellulose/TiO2/PANI composite nanofibers. Colloids Surf. A: Physicochem. Eng. Asp.2016, 494, 248–255.

    Article  CAS  Google Scholar 

  39. Lin, Q. Q.; Li, Y.; Yang, M. J. Tin oxide/graphene composite fabricated via a hydrothermal method for gas sensors working at room temperature. Sens. Actuators B: Chem.2012, 173, 139–147.

    Article  CAS  Google Scholar 

  40. Feng, Q. X.; Li, X. G; Wang, J.; Gaskov, A. M. Reduced graphene oxide (rGO) encapsulated Co3O4 composite nanofibers for highly selective ammonia sensors. Sens. Actuators B: Chem.2016, 222, 864–870.

    Article  CAS  Google Scholar 

  41. Maity, A.; Raychaudhuri, A. K.; Ghosh, B. High sensitivity NH3 gas sensor with electrical readout made on paper with perovskite halide as sensor material. Sci. Rep.2019, 9, 7777.

    Article  CAS  Google Scholar 

  42. Aba, L.; Yusuf, Y.; Mitrayana; Siswanta, D.; Junaidi; Triyana, K. Sensitivity improvement of ammonia gas sensor based on poly(3,4-ethylenedioxythiophene): Poly(styrenesulfonate) by employing doping of bromocresol green. J. Nanotechnol.2014, 2014, 864274.

    Article  CAS  Google Scholar 

  43. Rigoni, F.; Drera, G.; Pagliara, S.; Goldoni, A.; Sangaletti, L. High sensitivity, moisture selective, ammonia gas sensors based on single-walled carbon nanotubes functionalized with indium tin oxide nanoparticles. Carbon2014, 80, 356–363.

    Article  CAS  Google Scholar 

  44. Gouma, P.; Kalyanasundaram, K.; Yun, X.; Stanacevic, M.; Wang, L. S. Nanosensor and breath analyzer for ammonia detection in exhaled human breath. IEEE Sens. J.2010, 10, 49–53.

    Article  CAS  Google Scholar 

  45. Yao, J.; Jin, Z.; Zhong, L.; Natelson, D.; Tour, J. M. Two-terminal nonvolatile memories based on single-walled carbon nanotubes. ACS Nano2009, 3, 4122–4126.

    Article  CAS  Google Scholar 

  46. Yimit, A.; Itoh, K.; Murabayashi, M. Detection of ammonia in the ppt range based on a composite optical waveguide pH sensor. Sens. Actuators B: Chem.2003, 88, 239–245.

    Article  CAS  Google Scholar 

  47. Lovley, D. R. Electrically conductive pili: Biological function and potential applications in electronics. Curr. Opin. Electrochem.2017, 4, 190–198.

    Article  CAS  Google Scholar 

  48. Lovley, D. R. e-Biologics: Fabrication of sustainable electronics with “green” biological materials. mBio2017, 8, e00695–17.

    Article  CAS  Google Scholar 

  49. Adhikari, R. Y.; Malvankar, N. S.; Tuominen, M. T.; Lovley, D. R. Conductivity of individual Geobacter pili. RSC Adv.2016, 6, 8354–8357.

    Article  CAS  Google Scholar 

  50. Sun, Y. L.; Tang, H. Y.; Ribbe, A.; Duzhko, V.; Woodard, T. L.; Ward, J. E.; Bai, Y.; Nevin, K. P.; Nonnenmann, S. S.; Russell, T. et al. Conductive composite materials fabricated from microbially produced protein nanowires. Small2018, 14, 1802624.

    Article  CAS  Google Scholar 

  51. Kumar, A.; Holuszko, M.; Espinosa, D. C. R. E-waste: An overview on generation, collection, legislation and recycling practices. Resour. Conserv. Recycl.2017, 122, 32–42.

    Article  Google Scholar 

  52. Tansel, B. From electronic consumer products to e-wastes: Global outlook, waste quantities, recycling challenges. Environ. Int.2017, 98, 35–45.

    Article  Google Scholar 

  53. Tan, Y.; Adhikari, R. Y.; Malvankar, N. S.; Ward, J. E.; Woodard, T. L.; Nevin, K. P.; Lovley, D. R. Expressing the Geobacter metallireducens PilA in Geobacter sulfurreducens yields pili with exceptional conductivity. mBio2017, 8, e02203–16.

    Article  CAS  Google Scholar 

  54. Feng, J.; Peng, L. L.; Wu, C. Z.; Sun, X.; Hu, S. L.; Lin, C. W.; Dai, J.; Yang, J. L.; Xie, Y. Giant moisture responsiveness of VS2 ultrathin nanosheets for novel touchless positioning interface. Adv. Mater.2012, 24, 1969–1974.

    Article  CAS  Google Scholar 

  55. Liu, X. M.; Gao, H. Y.; Ward, J. E.; Liu, X. R.; Yin, B.; Fu, T. D.; Chen, J. H.; Lovley, D. R.; Yao, J. Power generation from ambient humidity using protein nanowires. Nature2020, 578, 550–554.

    Article  CAS  Google Scholar 

  56. Cui, S. M.; Pu, H. H.; Wells, S. A.; Wen, Z. H.; Mao, S.; Chang, J. B.; Hersam, M. C.; Chen, C. H. Ultrahigh sensitivity and layer-dependent sensing performance of phosphorene-based gas sensors. Nat. Commun.2015, 6, 8632.

    Article  CAS  Google Scholar 

  57. Donarelli, M.; Ottaviano, L. 2D materials for gas sensing applications: A review on graphene oxide, MoS2, WS2 and phosphorene. Sensors2018, 18, 3638.

    Article  CAS  Google Scholar 

  58. Jian, J. M.; Guo, X. S.; Lin, L. W.; Cai, Q.; Cheng, J.; Li, J. P. Gassensing characteristics of dielectrophoretically assembled composite film of oxygen plasma-treated SWCNTs and PEDOT/PSS polymer. Sens. Actuators B: Chem.2013, 178, 279–288.

    Article  CAS  Google Scholar 

  59. Pandey, S.; Nanda, K. K. Au nanocomposite based chemiresistive ammonia sensor for health monitoring. ACS Sensors2016, 1, 55–62.

    Article  CAS  Google Scholar 

  60. Suri, K.; Annapoorni, S.; Sarkar, A. K.; Tandon, R. P. Gas and humidity sensors based on iron oxide-polypyrrole nanocomposites. Sens. Actuators B: Chem.2002, 81, 277–282.

    Article  CAS  Google Scholar 

  61. Bi, H. C.; Yin, K. B.; Xie, X.; Ji, J.; Wan, S.; Sun, L. T.; Terrones, M.; Dresselhaus, M. S. Ultrahigh humidity sensitivity of graphene oxide. Sci. Rep.2013, 3, 2714.

    Article  Google Scholar 

  62. Xiao, K.; Malvankar, N. S.; Shu, C. J.; Martz, E.; Lovley, D. R.; Sun, X. Low energy atomic models suggesting a pilus structure that could account for electrical conductivity of Geobacter sulfurreducens pili. Sci. Rep.2016, 6, 23385.

    Article  CAS  Google Scholar 

  63. Feliciano, G. T.; Steidl, R. J.; Reguera, G. Structural and functional insights into the conductive pili of Geobacter sulfurreducens revealed in molecular dynamics simulations. Phys. Chem. Chem. Phys.2015, 17, 22217–22226.

    Article  CAS  Google Scholar 

  64. Philip, B.; Abraham, J. K.; Chandrasekhar, A.; Varadan, V. K. Carbon nanotube/PMMA composite thin films for gas-sensing applications. Smart Mater. Struct.2003, 12, 935–939.

    Article  CAS  Google Scholar 

  65. Li, C.; Zhang, D. H.; Liu, X. L.; Han, S.; Tang, T.; Han, J.; Zhou, C. W. In2O3 nanowires as chemical sensors. Appl. Phys. Lett.2013, 82, 1613.

    Article  CAS  Google Scholar 

  66. Tang, S. B.; Cao, Z. X. Adsorption and dissociation of ammonia on graphene oxides: A first-principles study. J. Phys. Chem. C2012, 116, 8778–8791.

    Article  CAS  Google Scholar 

  67. Malvankar, N. S.; Vargas, M.; Nevin, K. P.; Franks, A. E.; Leang, C.; Kim, B. C.; Inoue, K.; Mester, T.; Covalla, S. F.; Johnson, J. P. et al. Tunable metallic-like conductivity in microbial nanowire networks. Nat. Nanotechnol.2011, 6, 573–579.

    Article  Google Scholar 

  68. Lechner, B. A. J.; Kim, Y.; Feibelman, P. J.; Henkelman, G.; Kang, H.; Salmeron, M. Solvation and reaction of ammonia in molecularly thin water films. J. Phys. Chem. C2015, 119, 23052–23058.

    Article  CAS  Google Scholar 

  69. Lim, D. W.; Sadakiyo, M.; Kitagawa, H. Proton transfer in hydrogenbonded degenerate systems of water and ammonia in metal-organic frameworks. Chem. Sci.2019, 10, 16–33.

    Article  CAS  Google Scholar 

  70. Ueki, T.; Walker, D. J. F.; Woodard, T. L.; Nevin, K. P.; Nonnenmann, S. S.; Lovley, D. R. An escherichia coli chassis for production of electrically conductive protein nanowires. ACS Synth. Biol.2020, 9, 647–654.

    Article  CAS  Google Scholar 

  71. Yin, B.; Liu, X. M.; Gao, H. Y.; Fu, T. D.; Yao, J. Bioinspired and bristled microparticles for ultrasensitive pressure and strain sensors. Nat. Commun.2018, 9, 5161.

    Article  CAS  Google Scholar 

  72. Ueki, T.; Walker, D. J. F.; Tremblay, P. L.; Nevin, K. P.; Ward, J. E.; Woodard, T. L.; Nonnenmann, S. S.; Lovley, D. R. Decorating microbially produced protein nanowires with peptide ligands. ACS Synth. Biol.2019, 8, 1809–1817.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

J. Y. and D. R. L. acknowledge support from a seed fund through the Office of Technology Commercialization and Ventures at the University of Massachusetts, Amherst. J. Y. acknowledges the support from a National Science Foundation (NSF) Award ECCS-1917630. J. M. J. acknowledges support from a NSF grants CAREER CMMI1842308. A. F. S. acknowledges the support from a NSF Graduate Research Fellowship (No. S12100000000937). Part of the device fabrication work was conducted in the clean room of the Center for Hierarchical Manufacturing (CHM), an NSF Nanoscale Science and Engineering Center (NSEC) located at the University of Massachusetts, Amherst.

Author information

Authors and Affiliations

  1. Department of Biomedical Engineering, University of Massachusetts, Amherst, MA, 01003, USA

    Alexander F. Smith, Juan M. Jiménez & Jun Yao

  2. Department of Electrical and Computer Engineering, University of Massachusetts, Amherst, MA, 01003, USA

    Xiaomeng Liu, Tianda Fu & Jun Yao

  3. Department of Microbiology, University of Massachusetts, Amherst, MA, 01003, USA

    Trevor L. Woodard & Derek R. Lovley

  4. Department of Polymer Science and Engineering, University of Massachusetts, Amherst, MA, 01003, USA

    Todd Emrick

  5. Department of Mechanical and Industrial Engineering, University of Massachusetts, Amherst, MA, 01003, USA

    Juan M. Jiménez

  6. Institute for Applied Life Sciences (IALS), University of Massachusetts, Amherst, MA, 01003, USA

    Juan M. Jiménez, Derek R. Lovley & Jun Yao

Authors
  1. Alexander F. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaomeng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Trevor L. Woodard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tianda Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Todd Emrick
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juan M. Jiménez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Derek R. Lovley
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jun Yao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Derek R. Lovley or Jun Yao.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Smith, A.F., Liu, X., Woodard, T.L. et al. Bioelectronic protein nanowire sensors for ammonia detection. Nano Res. 13, 1479–1484 (2020). https://doi.org/10.1007/s12274-020-2825-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-020-2825-6

Keywords

Search

Navigation