AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Powered by AMiner. Clicking this button will take you away from SciOpen.
Home Nano Research Article
Article Link
Cite
EndNote(RIS) BibTeX
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Bioelectronic protein nanowire sensors for ammonia detection

Alexander F. Smith1, Xiaomeng Liu2, Trevor L. Woodard3, Tianda Fu2, Todd Emrick4, Juan M. Jiménez1,5,6, Derek R. Lovley3,6( ), Jun Yao1,2,6( )
Department of Biomedical Engineering, University of Massachusetts, Amherst, MA 01003, USA
Department of Electrical and Computer Engineering, University of Massachusetts, Amherst, MA 01003, USA
Department of Microbiology, University of Massachusetts, Amherst, MA 01003, USA
Department of Polymer Science and Engineering, University of Massachusetts, Amherst, MA 01003, USA
Department of Mechanical and Industrial Engineering, University of Massachusetts, Amherst, MA 01003, USA
Institute for Applied Life Sciences (IALS), University of Massachusetts, Amherst, MA 01003, USA
Show Author Information

Graphical Abstract

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.

Keywords

nanowireprotein nanowirebiomaterialbioelectronicsbiosensorammonia sensor

Electronic Supplementary Material

Download File(s)
12274_2020_2825_MOESM1_ESM.pdf (1.6 MB)

References

[1]
Kwak, D.; Lei, Y.; Maric, R. Ammonia gas sensors: A comprehensive review. Talanta 2019, 204, 713-720.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref Google Scholar
[6]
Kharitonov, S. A.; Barnes, P. J. Biomarkers of some pulmonary diseases in exhaled breath. Biomarkers 2002, 7, 1-32.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref Google Scholar
[12]
Mathew, T. L.; Pownraj, P.; Abdulla, S.; Pullithadathil, B. Technologies for clinical diagnosis using expired human breath analysis. Diagnostics 2015, 5, 27-60.
Crossref 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.
Crossref 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 One 2017, 12, e0178745.
Crossref Google Scholar
[15]
Sawicka, K.; Gouma, P.; Simon, S. Electrospun biocomposite nanofibers for urea biosensing. Sens. Actuators B: Chem .2005, 108, 585-588.
Crossref 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. USA 2001, 98, 4617-4621.
Crossref 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.
Crossref Google Scholar
[18]
Turner, A. P. F. Biosensors: Sense and sensibility. Chem. Soc. Rev 2013, 42, 3184-3196.
Crossref 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.
Crossref 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.
Crossref Google Scholar
[21]
Chopra, S.; Pham, A.; Gaillard, J.; Parker, A.; Rao, A. M. Carbon-nanotube-based resonant-circuit sensor for ammonia. Appl. Phys. Lett .2002, 80, 4632-4634.
Crossref 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.
Crossref 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.
Crossref 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 Solidi 2007, 204, 1820-1824.
Crossref 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. Nnanotechnology 2017, 28, 255502.
Crossref 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.
Crossref 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. Nanotechnology 2011, 22, 355501.
Crossref 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.
Crossref 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.
[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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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. Carbon 2014, 80, 356-363.
Crossref 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.
Crossref 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 Nano 2009, 3, 4122-4126.
Crossref 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.
Crossref Google Scholar
[47]
Lovley, D. R. Electrically conductive pili: Biological function and potential applications in electronics. Curr. Opin. Electrochem .2017, 4, 190-198.
Crossref Google Scholar
[48]
Lovley, D. R. e-Biologics: Fabrication of sustainable electronics with “green” biological materials. mBio 2017, 8, e00695-17.
Crossref 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.
Crossref 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. Small 2018, 14, 1802624.
Crossref 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.
Crossref Google Scholar
[52]
Tansel, B. From electronic consumer products to e-wastes: Global outlook, waste quantities, recycling challenges. Environ. Int .2017, 98, 35-45.
Crossref 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. mBio 2017, 8, e02203-16.
Crossref 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.
Crossref 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. Nature 2020, 578, 550-554.
Crossref 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.
Crossref Google Scholar
[57]
Donarelli, M.; Ottaviano, L. 2D materials for gas sensing applications: A review on graphene oxide, MoS2, WS2 and phosphorene. Sensors 2018, 18, 3638.
Crossref Google Scholar
[58]
Jian, J. M.; Guo, X. S.; Lin, L. W.; Cai, Q.; Cheng, J.; Li, J. P. Gas-sensing characteristics of dielectrophoretically assembled composite film of oxygen plasma-treated SWCNTs and PEDOT/PSS polymer. Sens. Actuators B: Chem .2013, 178, 279-288.
Crossref Google Scholar
[59]
Pandey, S.; Nanda, K. K. Au nanocomposite based chemiresistive ammonia sensor for health monitoring. ACS Sensors 2016, 1, 55-62.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref 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 .20013, 82, 1613.
Crossref Google Scholar
[66]
Tang, S. B.; Cao, Z. X. Adsorption and dissociation of ammonia on graphene oxides: A first-principles study. J. Phys. Chem. C 2012, 116, 8778-8791.
Crossref 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.
Crossref 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. C 2015, 119, 23052-23058.
Crossref Google Scholar
[69]
Lim, D. W.; Sadakiyo, M.; Kitagawa, H. Proton transfer in hydrogen-bonded degenerate systems of water and ammonia in metal-organic frameworks. Chem. Sci .2019, 10, 16-33.
Crossref 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.
Crossref 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.
Crossref 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.
Crossref Google Scholar
Nano Research
Volume 13 Issue 5,
May 2020
Pages 1479-1484
DOI: 10.1007/s12274-020-2825-6
Cite this article:
Smith AF, Liu X, Woodard TL, et al. Bioelectronic protein nanowire sensors for ammonia detection. Nano Research, 2020, 13(5): 1479-1484. https://doi.org/10.1007/s12274-020-2825-6
Topics:
Gas industryMedical applicationsNanosensors NanowiresProteins

937

Views

55

Crossref

N/A

Web of Science

56

Scopus

0

CSCD

Altmetrics
Received: 20 February 2020
Revised: 07 April 2020
Accepted: 19 April 2020
Published: 11 May 2020
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2020
Return