A self-powered biosensor based on triboelectric nanogenerator for dual-specificity bacterial detection

Abstract

Pathogenic and corrosive bacteria pose a significant risk to human health or economic well-being. The specific, sensitive, and on-site detection of these bacteria is thus of paramount significance but remains challenging. Taking inspiration from immunoassays with primary and secondary antibodies, we describe here a rational design of microbial sensor (MS) under a dual-specificity recognition strategy using Pseudomonas aeruginosa (P. aeruginosa) as the detection model. In the MS, engineered aptamers are served as the primary recognition element, while polydopamine-N-acetyl-D-galactosamine (PDA-Gal NAc) nanoparticles are employed as the secondary recognition element, which will also generate and amplify changes in the output voltage signal. To achieve self-powering capability, the MS is constructed based on a triboelectric nanogenerator (TENG) with the specific aptamers immobilized on the TENG electrode surface. The as-prepared MS-TENG system exhibits good stability in output performance under external forces, and high specificity toward P. aeruginosa, with no cross-reactivity observed. A linear relationship (R² = 0.995) between the output voltage and P. aeruginosa concentration is established, with a limit of detection estimated at around 8.7 × 10³ CFU mL⁻¹. The utilization of PDA-Gal NAc nanoparticles is found to play an important role in enhancing the specific and reliability of detection, and the underlying mechanisms are further clarified by computational simulations. In addition, the MS-TENG integrates a wireless communication module, enabling real-time monitoring of bacterial concentration on mobile devices. This work introduces a pioneering approach to designing self-powered smart microbial sensors with high specificity, using a double recognition strategy applicable to various bacteria beyond P. aeruginosa.

Keywords

bacterial detection / high specificity / microbial sensor / triboelectric nanogenerator / wireless transmission

References

[1] Guo L, Zhao P, Jia Y, et al. Inactivation of airborne pathogenic microorganisms by plasma-activated nebulized mist. J Hazard Mater. 2023;459:132072.

[2] Chen L, Zhang L, Xie Y, et al. Confronting antifungal resistance, tolerance, and persistence: advances in drug target discovery and delivery systems. Adv Drug Deliv Rev. 2023;200:115007.

[3] Guo N, Wang Y, Hui X, et al. Marine bacteria inhibit corrosion of steel via synergistic biomineralization. J Mater Sci Technol. 2021;66:82-90.

[4] Nnachi RC, Sui N, Ke B, et al. Biosensors for rapid detection of bacterial pathogens in water, food and environment. Environ Int. 2022;166:107357.

[5] Dehghani MH, Karri RR, Koduru JR, et al. Recent trends in the applications of sonochemical reactors as an advanced oxidation process for the remediation of microbial hazards associated with water and wastewater: a critical review. Ultrason Sonochem. 2023;94:106302.

[6] Sun W, Jing Z. Migration of rare and abundant species, assembly mechanisms, and ecological networks of microbiomes in drinking water treatment plants: effects of different treatment processes. J Hazard Mater. 2023;457:131726.

[7] Alafeef M, Moitra P, Pan D. Nano-enabled sensing approaches for pathogenic bacterial detection. Biosens Bioelectron. 2020;165:112276.

[8] Xu D, Gu T, Lovley DR. Microbially mediated metal corrosion. Nat Rev Microbiol. 2023;21(11):705-718.

[9] Chugh B, Sheetal, Singh M, et al. Extracellular electron transfer by Pseudomonas aeruginosa in biocorrosion: a review. ACS Biomater Sci Eng. 2022;8(3):1049-1059.

[10] Lim GM, Kim JK, Kim EJ, et al. Generation of a recombinant antibody for sensitive detection of Pseudomonas aeruginosa. BMC Biotechnol. 2022;22(1):21.

[11] Li Z, Huang L, Hao W, Yang J, Qian H, Zhang D. Accelerating effect of pyocyanin on microbiologically influenced corrosion of 304 stainless steel by the Pseudomonas aeruginosa biofilm. Bioelectrochemistry. 2022;146:108130.

[12] Curran CS, Bolig T, Torabi-Parizi P. Mechanisms and targeted therapies for Pseudomonas aeruginosa lung infection. Am J Respir Crit Care Med. 2018;197(6):708-727.

[13] Zhang Z, Sun Y, Yang Y, et al. Rapid identification and monitoring of multiple bacterial infections using printed nanoarrays. Adv Mater. 2023;35(12):e2211363.

[14] Zhu J, Wang B, Zhang Y, Wei T, Gao T. Living electrochemical biosensing: engineered electroactive bacteria for biosensor development and the emerging trends. Biosens Bioelectron. 2023;237:115480.

[15] Liu G, Lv Z, Batool S, et al. Biocompatible material-based flexible biosensors: from materials design to wearable/implantable devices and integrated sensing systems. Small. 2023;19(27):e2207879.

[16] Xu X, Lin X, Wang L, Ma Y, Sun T, Bian X. A novel dual bacteria-imprinted polymer sensor for highly selective and rapid detection of pathogenic bacteria. Biosensors. 2023;13(9):868.

[17] Zahraee H, Mehrzad A, Abnous K, Chen CH, Khoshbin Z, Verdian A. Recent advances in aptasensing strategies for monitoring phycotoxins: promising for food safety. Biosensors (Basel). 2022;13(1):56.

[18] Pandey A, Gurbuz Y, Ozguz V, Niazi JH, Qureshi A. Graphene-interfaced electrical biosensor for label-free and sensitive detection of foodborne pathogenic E. coli O157:H7. Biosens Bioelectron. 2017;91:225-231.

[19] Huang CW, Lin C, Nguyen MK, Hussain A, Bui XT, Ngo HH. A review of biosensor for environmental monitoring: principle, application, and corresponding achievement of sustainable development goals. Bioengineered. 2023;14(1):58-80.

[20] Yuan J, Zhao K, Tan X, et al. Perspective on the development of synthetic microbial community (SynCom) biosensors. Trends Biotechnol. 2023;41(10):1227-1236.

[21] Wu L, Wang Y, Xu X, et al. Aptamer-based detection of circulating targets for precision medicine. Chem Rev. 2021;121(19):12035-12105.

[22] Wang Y, Liu X, Wu L, et al. Construction and bioapplications of aptamer-based dual recognition strategy. Biosens Bioelectron. 2022;195:113661.

[23] Chen HM, Jheng KR, Yu AD. Direct, label-free, selective, and sensitive microbial detection using a bacteriorhodopsin-based photoelectric immunosensor. Biosens Bioelectron. 2017;91:24-31.

[24] Wang Z, Cai R, Gao Z, Yuan Y, Yue T. Immunomagnetic separation: an effective pretreatment technology for isolation and enrichment in food microorganisms detection. Compr Rev Food Sci Food Saf. 2020;19(6):3802-3824.

[25] Zhang N, Li J, Liu B, et al. Signal enhancing strategies in aptasensors for the detection of small molecular contaminants by nanomaterials and nucleic acid amplification. Talanta. 2022;236:122866.

[26] Yu H, Zhu J, Shen G, Deng Y, Geng X, Wang L. Improving aptamer performance: key factors and strategies. Mikrochim Acta. 2023;190(7):255.

[27] Liu B, Liu J, Hu X, et al. Recent advances in aptamer-based therapeutic strategies for targeting cancer stem cells. Mater Today Bio. 2023;19:100605.

[28] Fu L, Deng S, Luo Y, Fu Q, Fan Y, Jia L. An ultrasensitive colorimetric biosensor for the detection of Gram-positive bacteria by integrating paper-based enrichment and carbon dot-based selective recognition. Talanta. 2023;265:124920.

[29] Fu L, Chen Q, Jia L. Carbon dots and gold nanoclusters assisted construction of a ratiometric fluorescent biosensor for detection of Gram-negative bacteria. Food Chem. 2022;374:131750.

[30] Wang C, Wang P, Li J, et al. Utilizing parasitic capacitance of single-droplet electricity generator for specific bacterial detection. Adv Funct Mater. 2023;33(37):2302524.

[31] Ching J, Osborne A, Eva R, Prudent J, Yu-Wai-Man P. Quantifying inter-organelle membrane contact sites using proximity ligation assay in fixed optic nerve sections. Exp Eye Res. 2021;213:108793.

[32] Cai Y, Yan J, Zhu L, Wang H, Lu Y. A rapid immunochromatographic method based on a secondary antibody-labelled magnetic nanoprobe for the detection of hepatitis B preS2 surface antigen. Biosensors (Basel). 2020;10(11):161.

[33] Li S, Zhang Y, Wang Y, et al. Physical sensors for skin-inspired electronics. InfoMat. 2019;2(1):184-211.

[34] Wang C, Guo H, Wang P, Li J, Sun Y, Zhang D. An advanced strategy to enhance TENG output: reducing triboelectric charge decay. Adv Mater. 2023;35(17):e2209895.

[35] Zhou Z, Wang P, Li J, et al. A self-powered microbiosensor system for specific bacteria detection based on triboelectric nanogenerator. Nano Energy. 2022;98:107317.

[36] Wang C, Wang P, Chen J, et al. Self-powered biosensing system driven by triboelectric nanogenerator for specific detection of Gram-positive bacteria. Nano Energy. 2022;93:106828.

[37] Feng J, Zhou H, Cao Z, et al. 0.5 m triboelectric nanogenerator for efficient blue energy harvesting of all-sea areas. Adv Sci (Weinh). 2022;9(35):e2204407.

[38] Shen J, Li B, Yang Y, et al. Application, challenge and perspective of triboelectric nanogenerator as micro-nano energy and self-powered biosystem. Biosens Bioelectron. 2022;216:114595.

[39] Xu C, Yu J, Huo Z, Wang Y, Sun Q, Wang ZL. Pursuing the tribovoltaic effect for direct-current triboelectric nanogenerators. Energy Environ Sci. 2023;16(3):983-1006.

[40] Chen J, Li J, Wang P, et al. Utilizing breakdown discharge of self-powered triboelectric nanogenerator to realize multimodal sterilization. Adv Sustain Syst. 2022;7(3):2370007.

[41] Wang W, Pang J, Su J, et al. Applications of nanogenerators for biomedical engineering and healthcare systems. InfoMat. 2021;4(2):e12262.

[42] Niu H, Yin F, Kim ES, et al. Advances in flexible sensors for intelligent perception system enhanced by artificial intelligence. InfoMat. 2023;5(5):e12412.

[43] Shanina E, Siebs E, Zhang H, et al. Protein-observed 19F NMR of LecA from Pseudomonas aeruginosa. Glycobiology. 2021;31(2):159-165.

[44] Boffoli D, Bellato F, Avancini G, et al. Tobramycin-loaded complexes to prevent and disrupt Pseudomonas aeruginosa biofilms. Drug Deliv Transl Res. 2022;12(8):1788-1810.

[45] Jiang P, Zhang L, Guo H, et al. Signal output of triboelectric nanogenerator at oil–water–solid multiphase interfaces and its application for dual-signal chemical sensing. Adv Mater. 2019;31(39):1902793.

[46] Hu L, Cheng J, Li Y, Liu J, Zhou J, Cen K. Amino-functionalized surface modification of polyacrylonitrile hollow fiber-supported polydimethylsiloxane membranes. Appl Surf Sci. 2017;413:27-34.

[47] Le TN, Lee CK. Surface functionalization of poly(N-vinylpyrrolidone) onto poly(dimethylsiloxane) for anti-biofilm application. Appl Biochem Biotechnol. 2020;191(1):29-44.

[48] Batul R, Yu A, Bhave M, Khaliq A. Synthesis of polydopamine nanoparticles for drug delivery applications. Microsc Microanal. 2018;24(S1):1758-1759.

[49] Hu D, Zou L, Li B, Hu M, Ye W, Ji J. Photothermal killing of methicillin-resistant Staphylococcus aureus by bacteria-targeted polydopamine nanoparticles with nano-localized hyperpyrexia. ACS Biomater Sci Eng. 2019;5(10):5169-5179.

[50] Yu B, Liu J, Liu S, Zhou F. Pdop layer exhibiting zwitterionicity: a simple electrochemical interface for governing ion permeability. Chem Commun (Camb). 2010;46(32):5900-5902.

[51] Ding L, Gao J, Chung T-S. Schiff base reaction assisted one-step self-assembly method for efficient gravity-driven oil–water emulsion separation. Sep Purif Technol. 2019;213:437-446.

[52] Nan Y, Shao J, Willatzen M, Wang ZL. Understanding contact electrification at water/polymer interface. Research (Wash D C). 2022;2022:9861463.

[53] Menge HG, Huynh ND, Hwang HJ, Han S, Choi D, Park YT. Designable skin-like triboelectric nanogenerators using layer-by-layer self-assembled polymeric nanocomposites. ACS Energy Lett. 2021;6(7):2451-2459.

[54] Menge HG, Huynh ND, Choi K, Cho C, Choi D, Park YT. Body-patchable, antimicrobial, encodable TENGs with ultrathin, free-standing, translucent chitosan/alginate/silver nanocomposite multilayers. Adv Funct Mater. 2022;33(7):2210571.

[55] Ding P, Chen J, Farooq U, et al. Realizing the potential of polyethylene oxide as new positive tribo-material: over 40 W/m² high power flat surface triboelectric nanogenerators. Nano Energy. 2018;46:63-72.

[56] Shahwan M, Khan MS, Husain FM, Shamsi A. Understanding binding between donepezil and human ferritin: molecular docking and molecular dynamics simulation approach. J Biomol Struct Dyn. 2022;40(9):3871-3879.

[57] Khan A, Mohammad T, Shamsi A, et al. Identification of plant-based hexokinase 2 inhibitors: combined molecular docking and dynamics simulation studies. J Biomol Struct Dyn. 2022;40(20):10319-10331.

[58] Ishak SNH, Aris S, Halim KBA, et al. Molecular dynamic simulation of space and earth-grown crystal structures of thermostable T1 lipase Geobacillus zalihae revealed a better structure. Molecules. 2017;22(10):1574.

[59] Cioci G, Mitchell EP, Gautier C, et al. Structural basis of calcium and galactose recognition by the lectin PA-IL of Pseudomonas aeruginosa. FEBS Lett. 2003;555(2):297-301.

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2023 2023 Institute of Oceanology, Chinese Academy of Sciences and The Authors. InfoMat published by UESTC and John Wiley & Sons Australia, Ltd.