journal article·2020-04Open access

Biofuel powered glucose detection in bodily fluids with an n-type conjugated polymer

David Ohayon, Georgios Nikiforidis, Achilleas Savva, Andrea Giugni, Shofarul Wustoni, Tamilarasan Palanisamy, Xingxing Chen, Iuliana Petruta Maria, Enzo Di Fabrizio, Pedro M. F. J. Costa, Iain McCulloch, Sahika Inal

Nature Materials· Volume 19· Issue 4

Abstract

A promising class of materials for applications that rely on electron transfer for signal generation are the n-type semiconducting polymers. Here we demonstrate the integration of an n-type conjugated polymer with a redox enzyme for the autonomous detection of glucose and power generation from bodily fluids. The reversible, mediator-free, miniaturized glucose sensor is an enzyme-coupled organic electrochemical transistor with a detection range of six orders of magnitude. This n-type polymer is also used as an anode and paired with a polymeric cathode in an enzymatic fuel cell to convert the chemical energy of glucose and oxygen into electrical power. The all-polymer biofuel cell shows a performance that scales with the glucose content in the solution and a stability that exceeds 30 days. Moreover, at physiologically relevant glucose concentrations and from fluids such as human saliva, it generates enough power to operate an organic electrochemical transistor, thus contributes to the technological advancement of self-powered micrometre-scale sensors and actuators that run on metabolites produced in the body.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Electrochemical sensors and biosensors · Conducting polymers and applications · Electrochemical Analysis and Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (45)

Show source-provided references
1. Pappa, A.-M. et al. Organic electronics for point-of-care metabolite monitoring. Trends Biotechnol. 36, 45–59 (2018).10.1016/j.tibtech.2017.10.022 ↗
2. Gifford, R. Continuous glucose monitoring: 40 years, what we’ve learned and what’s next. ChemPhysChem 14, 2032–2044 (2013).10.1002/cphc.201300172 ↗
3. Witkowska Nery, E., Kundys, M., Jeleń, P. S. & Jönsson-Niedziółka, M. Electrochemical glucose sensing: is there still room for improvement? Anal. Chem. 88, 11271–11282 (2016).10.1021/acs.analchem.6b03151 ↗
4. Wang, J. Electrochemical glucose biosensors. Chem. Rev. 108, 814–825 (2008).10.1021/cr068123a ↗
5. Heller, A. & Feldman, B. Electrochemical glucose sensors and their applications in diabetes management. Chem. Rev. 108, 2482–2505 (2008).10.1021/cr068069y ↗
6. Wu, Y. & Hu, S. Biosensors based on direct electron transfer in redox proteins. Microchim. Acta 159, 1–17 (2007).10.1007/s00604-007-0749-4 ↗
7. Zhang, W. & Li, G. Third-generation biosensors based on the direct electron transfer of proteins. Anal. Sci. 20, 603–609 (2004).10.2116/analsci.20.603 ↗
8. Zhu, C., Yang, G., Li, H., Du, D. & Lin, Y. Electrochemical sensors and biosensors based on nanomaterials and nanostructures. Anal. Chem. 87, 230–249 (2015).10.1021/ac5039863 ↗
9. Kissinger, P. T. Engineering the bioelectronic interface: applications to analyte biosensing and protein detection. J. Am. Chem. Soc. 132, 1444–1444 (2010).10.1021/ja9108648 ↗
10. Banica, F. G. Chemical Sensors and Biosensors: Fundamentals and Applications (Wiley, 2012).10.1002/9781118354162 ↗
11. Simon, D. T., Gabrielsson, E. O., Tybrandt, K. & Berggren, M. Organic bioelectronics: bridging the signaling gap between biology and technology. Chem. Rev. 116, 13009–13041 (2016).10.1021/acs.chemrev.6b00146 ↗
12. Luz, R. A. S., Pereira, A. R., de Souza, J. C. P., Sales, F. C. P. F. & Crespilho, F. N. Enzyme biofuel cells: thermodynamics, kinetics and challenges in applicability. ChemElectroChem 1, 1751–1777 (2014).10.1002/celc.201402141 ↗
13. Minteer, S. D., Atanassov, P., Luckarift, H. R. & Johnson, G. R. New materials for biological fuel cells. Mater. Today 15, 166–173 (2012).10.1016/S1369-7021(12)70070-6 ↗
14. Aghahosseini, H. et al. Glucose-based biofuel cells: nanotechnology as a vital science in biofuel cells performance. Nanochem. Res. 1, 183–204 (2016).
15. Kwon, C. H. et al. High-power hybrid biofuel cells using layer-by-layer assembled glucose oxidase-coated metallic cotton fibers. Nat. Commun. 9, 4479 (2018).10.1038/s41467-018-06994-5 ↗
16. Wen, D. & Eychmüller, A. Enzymatic biofuel cells on porous nanostructures. Small 12, 4649–4661 (2016).10.1002/smll.201600906 ↗
17. Giovannitti, A. et al. The role of the side chain on the performance of n-type conjugated polymers in aqueous electrolytes. Chem. Mater. 30, 2945–2953 (2018).10.1021/acs.chemmater.8b00321 ↗
18. Inal, S., Rivnay, J., Suiu, A.-O., Malliaras, G. G. & McCulloch, I. Conjugated polymers in bioelectronics. Acc. Chem. Res. 51, 1368–1376 (2018).10.1021/acs.accounts.7b00624 ↗
19. Spyropoulos, G. D., Gelinas, J. N. & Khodagholy, D. Internal ion-gated organic electrochemical transistor: a building block for integrated bioelectronics. Sci. Adv. 5, eaau7378 (2019).10.1126/sciadv.aau7378 ↗
20. Pappa, A. M. et al. Direct metabolite detection with an n-type accumulation mode organic electrochemical transistor. Sci. Adv. 4, eaat0911 (2019).10.1126/sciadv.aat0911 ↗
21. Liao, C., Zhang, M., Niu, L., Zheng, Z. & Yan, F. Highly selective and sensitive glucose sensors based on organic electrochemical transistors with graphene-modified gate electrodes. J. Mater. Chem. B 1, 3820–3829 (2013).10.1039/c3tb20451k ↗
22. Piro, B. et al. Fabrication and use of organic electrochemical transistors for sensing of metabolites in aqueous media. Appl. Sci. 8, 928 (2018).10.3390/app8060928 ↗
23. Lineweaver, H. & Burk, D. The determination of enzyme dissociation constants. J. Am. Chem. Soc. 56, 658–666 (1934).10.1021/ja01318a036 ↗
24. Trefz, D. et al. Electrochemical investigations of the n-type semiconducting polymer P(NDI2OD-T2) and its monomer: new insights in the reduction behavior. J. Phys. Chem. C 119, 22760–22771 (2015).10.1021/acs.jpcc.5b05756 ↗
25. Wooten, M., Karra, S., Zhang, M. & Gorski, W. On the direct electron transfer, sensing, and enzyme activity in the glucose oxidase/carbon nanotubes system. Anal. Chem. 86, 752–757 (2014).10.1021/ac403250w ↗
26. Zhang, Y. et al. Visualizing the solid–liquid interface of conjugated copolymer films using fluorescent liposomes. ACS Appl. Bio Mater. 1, 1348–1354 (2018).10.1021/acsabm.8b00323 ↗
27. Giovannitti, A. et al. N-type organic electrochemical transistors with stability in water. Nat. Commun. 7, 13066 (2016).10.1038/ncomms13066 ↗
28. Giussani, E., Fazzi, D., Brambilla, L., Caironi, M. & Castiglioni, C. Molecular level investigation of the film structure of a high electron mobility copolymer via vibrational spectroscopy. Macromolecules 46, 2658–2670 (2013).10.1021/ma302664s ↗
29. Navarrete, J. T. L. & Zerbi, G. Lattice dynamics and vibrational spectra of polythiophene. II. Effective coordinate theory, doping induced, and photoexcited spectra. J. Chem. Phys. 94, 965–970 (1991).10.1063/1.459987 ↗
30. Mitraka, E. et al. Oxygen-induced doping on reduced PEDOT. J. Mater. Chem. A 5, 4404–4412 (2017).10.1039/C6TA10521A ↗
31. Singh, S. K., Crispin, X. & Zozoulenko, I. V. Oxygen reduction reaction in conducting polymer PEDOT: density functional theory study. J. Phys. Chem. C 121, 12270–12277 (2017).10.1021/acs.jpcc.7b03210 ↗
32. Winther-Jensen, B., Winther-Jensen, O., Forsyth, M. & MacFarlane, D. R. High rates of oxygen reduction over a vapor phase–polymerized PEDOT electrode. Science 321, 671–674 (2008).10.1126/science.1159267 ↗
33. Mitraka, E. et al. Electrocatalytic production of hydrogen peroxide with poly(3,4-ethylenedioxythiophene) electrodes. Adv. Sustain. Syst. 3, 1800110 (2019).10.1002/adsu.201800110 ↗
34. Eckermann, A. L., Feld, D. J., Shaw, J. A. & Meade, T. J. Electrochemistry of redox-active self-assembled monolayers. Coord. Chem. Rev. 254, 1769–1802 (2010).10.1016/j.ccr.2009.12.023 ↗
35. Salimi, A., Sharifi, E., Noorbakhsh, A. & Soltanian, S. Immobilization of glucose oxidase on electrodeposited nickel oxide nanoparticles: direct electron transfer and electrocatalytic activity. Biosens. Bioelectron. 22, 3146–3153 (2007).10.1016/j.bios.2007.02.002 ↗
36. Laviron, E. General expression of the linear potential sweep voltammogram in the case of diffusionless electrochemical systems. J. Electroanal. Chem. Interfacial Electrochem. 101, 19–28 (1979).10.1016/S0022-0728(79)80075-3 ↗
37. Liu, J. et al. Enhancing molecular n-type doping of donor–acceptor copolymers by tailoring side chains. Adv. Mater. 30, 1704630 (2018).10.1002/adma.201704630 ↗
38. Wang, S. et al. A chemically doped naphthalenediimide–bithiazole polymer for n-type organic thermoelectrics. Adv. Mater. 30, 1801898 (2018).10.1002/adma.201801898 ↗
39. Cho, C. et al. Completely organic multilayer thin film with thermoelectric power factor rivaling inorganic tellurides. Adv. Mater. 27, 2996–3001 (2015).10.1002/adma.201405738 ↗
40. Rivnay, J. et al. Unconventional face-on texture and exceptional in-plane order of a high mobility n-type polymer. Adv. Mater. 22, 4359–4363 (2010).10.1002/adma.201001202 ↗
41. Miglbauer, E., Wójcik, P. J. & Głowacki, E. D. Single-compartment hydrogen peroxide fuel cells with poly(3,4-ethylenedioxythiophene) cathodes. Chem. Commun. 54, 11873–11876 (2018).10.1039/C8CC06802J ↗
42. Savva, A. et al. Influence of water on the performance of organic electrochemical transistors. Chem. Mater. 31, 927–937 (2019).10.1021/acs.chemmater.8b04335 ↗
43. Wustoni, S. & Savva, A. & Sun, R. & Bihar, E. & Inal, S. Enzyme-free detection of glucose with a hybrid conductive gel electrode. Adv. Mater. Interfaces 6, 1800928 (2019).10.1002/admi.201800928 ↗
44. Savva, A. & Wustoni, S. & Inal. Ionic-to-electronic coupling efficiency in PEDOT:PSS films operated in aqueous electrolytes. J. Mater. Chem. C 6, 12023–12030 (2018).10.1039/C8TC02195C ↗
45. Bihar, E. et al. A fully inkjet-printed disposable glucose sensor on paper. npj Flexible Electron. 2, 30 (2018).10.1038/s41528-018-0044-y ↗