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Graphene-DNAzyme-based fluorescent biosensor for Escherichia coli detection

  • Meng Liu (a1) (a2) (a3), Qiang Zhang (a2) (a4), John D. Brennan (a1) (a2) and Yingfu Li (a1) (a2)

Abstract

Herein we describe the use of a new DNAzyme/graphene hybrid material as a biointerfaced sensing platform for optical detection of pathogenic bacteria. The hybrid consists of a colloidal graphene nanomaterial and an Escherichia coli-activated RNA-cleaving DNAzyme and is prepared via non-covalent self-assembly of the DNAzyme onto the graphene surface. Exposure of the hybrid material to E. coli-containing samples results in the release of the DNAzyme, followed by the cleavage-mediated production of a fluorescent signal. Given that specific RNA-cleaving DNAzymes can be created for diverse bacterial pathogens, direct interfacing of graphene materials with such DNAzymes represents a general and attractive approach for real-time, sensitive, and highly selective detection of pathogenic bacteria.

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Copyright

Corresponding author

Address all correspondence to John D. Brennan and Yingfu Li at liying@mcmaster.ca; brennanj@mcmaster.ca

References

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1.Centers for Disease Control and Prevention, CDC Estimates of Foodborne Illness in the United States, Website: http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html.
2.Su, H., Ma, Q., Shang, K., Liu, T., Yin, H., and Ai, S.: Gold nanoparticles as colorimetric sensor: a case study on E. coli O157:H7 as a model for Gram-negative bacteria. Sens. Actuators B. 161, 298303 (2012).
3.Belgrader, P., Benett, W., Hadley, D., Richards, J., Stratton, P., Mariella, R., and Milanovich, F.: PCR detection of bacteria in seven minutes. Science 284, 449450 (1999).
4.Ivnitski, D., Abdel-Hamid, I., Atanasov, P., and Wilkins, E.: Flow-through immunofiltration assay system for rapid detection of E. coli O157:H7. Biosens. Bioelectron. 14, 599624 (1999).
5.Jarvis, R.M. and Goodacre, R.: Discrimination of bacteria using surface-enhanced Raman spectroscopy. Anal. Chem. 76, 4047 (2004).
6.Oh, B.K., Lee, W., Chun, B.S., Bae, Y.M., Lee, W.H., and Choi, J.W.: The fabrication of protein chip based on surface plasmon resonance for detection of pathogens. Biosens. Bioelectron. 20, 18471850 (2005).
7.Wang, Z.F., Cheng, S., Ge, S.L., Wang, H., Wang, Q.J., He, P.G., and Fang, Y.Z.: Ultrasensitive detection of bacteria by microchip electrophoresis based on multiple-concentration approaches combining chitosan sweeping, field-amplified sample stacking, and reversed-field stacking. Anal. Chem. 84, 16871694 (2012).
8.Nicolaou, N., Xu, Y., and Goodacre, R.: Detection and quantification of bacterial spoilage in milk and pork meat using MALDI-TOF-MS and multivariate analysis. Anal. Chem. 84, 59515958 (2012).
9.Sanvicens, N., Pastells, C., Pascual, N., and Marco, M.P.: Nanoparticle-based biosensors for detection of pathogenic bacteria. Trends Anal. Chem. 28, 12431252 (2009).
10.Ray, P.C., Khan, S.A., Singh, A.K., Senapati, D., and Fan, Z.: Nanomaterials for targeted detection and photothermal killing of bacteria. Chem. Soc. Rev. 41, 31933209 (2012).
11.Massad-Ivanir, N., Shtenberg, G., Zeidman, T., and Segal, E.: Construction and characterization of porous SiO2/hydrogel hybrids as optical biosensors for rapid detection of bacteria. Adv. Funct. Mater. 20, 22692277 (2010).
12.Massad-Ivanir, N., Shtenberg, G., Tzur, A., Krepker, M.A., and Segal, E.: Engineering nanostructured porous SiO2 surfaces for bacteria detection via “direct cell capture”. Anal. Chem. 83, 32823289 (2011).
13.Hahn, M.A., Tabb, J.S., and Krauss, T.D.: Detection of single bacterial pathogens with semiconductor quantum dots. Anal. Chem. 77, 48614869 (2005).
14.Edgar, R., McKinstry, M., Hwang, J., Oppenheim, A.B., Fekete, R.A., Giulian, G., Merril, C., Nagashima, K., and Adhya, S.: High-sensitivity bacterial detection using biotin-tagged phage and quantum-dot nanocomplexes. Proc. Natl. Acad. Sci. USA 103, 48414845 (2006).
15.Wang, C. and Irudayaraj, J.: Gold nanorod probes for the detection of multiple pathogens. Small 4, 22042208 (2008).
16.Fu, J., Park, B., and Zhao, Y.: Limitation of a localized surface plasmon resonance sensor for Salmonella detection. Sens. Actuators B 141, 276283 (2009).
17.Singh, A.K., Senapati, D., Wang, S., Griffin, J., Neely, A., Candice, P., Naylor, K.M., Varisli, B., Kalluri, J.R., and Ray, P.C.: Gold nanorod based selective identification of Escherichia coli bacteria using two-photon Rayleigh scattering spectroscopy. ACS Nano 3, 19061912 (2009).
18.Xu, X., Chen, Y., Wei, H.J., Xia, B., Liu, F., and Li, N.: Counting bacteria using functionalized gold nanoparticles as the light-scattering reporter. Anal. Chem. 84, 97219728 (2012).
19.Premasiri, W.R., Moir, D.T., Klempner, M.S., Krieger, N., Jones, G., and Ziegler, L.D.: Characterization of the surface enhanced Raman scattering (SERS) of bacteria. J. Phys. Chem. B 109, 312320 (2005).
20.Kuo, W.S., Chang, C.N., Chang, Y.T., and Yeh, C.S.: Antimicrobial gold nanorods with dual-modality photodynamic inactivation and hyperthermia. Chem. Commun. 32, 48534855 (2009).
21.Kell, A.J., Stewart, G., Ryan, S., Peytavi, R., Boissinot, M., Huletsky, A., Bergeron, M., and Simard, B.: Vancomycin-modified nanoparticles for efficient targeting and preconcentration of Gram-positive and Gram-negative bacteria. ACS Nano 2, 17771788 (2008).
22.Lee, H., Yoon, T.J., and Weissleder, R.: Ultrasensitive detection of bacteria using core-shell nanoparticles and an NMR-filter system. Angew. Chem. Int. Ed. 48, 56575660 (2009).
23.Ravindranath, S.P., Mauer, L.J., Deb-Roy, C., and Irudayaraj, J.: Biofunctionalized magnetic nanoparticle integrated mid-infrared pathogen sensor for food matrixes. Anal. Chem. 81, 28402846 (2009).
24.Chung, H.J., Reiner, T., Budin, G., Min, C., Liong, M., Issadore, D., Lee, H., and Weissleder, R.: Ubiquitous detection of gram-positive bacteria with bioorthogonal magneto fluorescent nanoparticles. ACS Nano 5, 88348841 (2011).
25.Zelada-Guillén, G.A., Riu, J., Düzgün, A., and Rius, F.X.: Immediate detection of living bacteria at ultralow concentrations using a carbon nanotube based potentiometric aptasensor. Angew. Chem., Int. Ed. 48, 73347337 (2009).
26.Mannoor, M.S., Tao, H., Clayton, J.D., Sengupta, A., Kaplan, D.L., Naik, R.R., Verma, N., Omenetto, F.G., and McAlpine, M.C.: Graphene-based wireless bacteria detection on tooth enamel. Nat. Commun. 3, 763 (2012).
27.Sapsford, K.E., Algar, W.R., Berti, L., Gemmill, K.B., Casey, B.J., Oh, E., Stewart, M.H., and Medintz, I.L.: Functionalizing nanoparticles with biological molecules: developing chemistries that facilitate nanotechnology. Chem. Rev. 113, 19042074 (2013).
28.Algar, W. R., Prasuhn, D.E., Stewart, M.H., Jennings, T.L., Blanco-Canosa, J.B., Dawson, P.E., and Medintz, I.L.: The controlled display of biomolecules on nanoparticles: a challenge suited to bioorthogonal chemistry. Bioconjugate Chem. 22, 825858 (2011).
29.Soukka, T., Härmä, H., Paukkunen, J., and Lövgren, T.: Utilization of kinetically enhanced monovalent binding affinity by immunoassays based on multivalent nanoparticle-antibody bioconjugates. Anal. Chem. 73, 22542260 (2001).
30.Mann, J.A., Alava, T., Craighead, H.G., and Dichtel, W.R.: Preservation of antibody selectivity on graphene by conjugation to a tripod monolayer. Angew. Chem. Int. Ed. 52, 31773180 (2013).
31.Chen, L., Zhang, X., Zhou, G., Xiang, X., Ji, X., Zheng, Z., He, Z., and Wang, H.: Simultaneous determination of human enterovirus 71 and coxsackievirus B3 by dual-color quantum dots and homogeneous immunoassay. Anal. Chem. 84, 32003207 (2012).
32.Liu, M., Song, J., Shuang, S., Dong, C., Brennan, J.D., and Li, Y.: A graphene-based biosensing platform based on the release of DNA probes and rolling circle amplification. ACS Nano 8, 55645573 (2014).
33.Zhao, X.H., Kong, R.M., Zhang, X.B., Meng, H.M., Liu, W.N., Tan, W.H., Shen, G.L., and Yu, R.Q.: Graphene-DNAzyme based biosensor for amplified fluorescence “turn-on” detection of Pb2+ with a high selectivity. Anal. Chem. 83, 50625066 (2011).
34.Ali, M.M., Aguirre, S.D., Lazim, H., and Li, Y.: Fluorogenic DNAzyme probes as bacterial indicators. Angew. Chem. Int. Ed. 50, 37513754 (2011).
35.Shen, Z., Wu, Z., Chang, D., Zhang, W., Tram, K., Lee, C., Kim, P., Salena, B.J., and Li, Y.: A catalytic DNA activated by a specific strain of bacterial pathogen. Angew. Chem. Int. Ed. 55, 24312434 (2016).
36.He, S., Qu, L., Shen, Z., Tan, Y., Zeng, M., Liu, F., Jiang, Y., and Li, Y.: Highly specific recognition of breast tumors by an RNA-cleaving fluorogenic DNAzyme probe. Anal. Chem. 87, 569577 (2015).
37.Liu, M., Chang, D., and Li, Y.: Discovery and biosensing applications of diverse RNA-cleaving DNAzymes. Acc. Chem. Res. 50, 22732283 (2017).
38.Morrison, D., Rothenbroker, M., and Li, Y.: DNAzymes: selected for applications. Small Methods 2, 1700319 (2018).
39.Chen, D., Feng, H., and Li, J.H.: Graphene oxide: preparation, functionalization, and electrochemical applications. Chem. Rev. 112, 60276053 (2012).
40.Guo, S.J. and Dong, S.J.: Graphene and its derivative-based sensing materials for analytical devices. J. Mater. Chem. 21, 1850318516 (2011).
41.Feng, L.Y., Wu, L., and Qu, X.G.: New horizons for diagnostics and therapeutic applications of graphene and graphene oxide. Adv. Mater. 25, 168186 (2013).
42.Varghese, N., Mogera, U., Govindaraj, A., Das, A., Maiti, P.K., Sood, A.K., and Rao, C.N.R.: Binding of DNA nucleobases and nucleosides with graphene. Chem. Phys. Chem. 10, 206210 (2009).
43.Morales-Narváez, E., and Merkoçi, A.: Graphene oxide as an optical biosensing platform. Adv. Mater. 24, 32983308 (2012).
44.Kochmann, S., Hirsch, T., and Wolfbeis, O.S.: Graphenes in chemical sensors and biosensors. Trends Anal. Chem. 39, 87113 (2012).
45.Swathi, R.S. and Sebastian, K.L.: Resonance energy transfer from a dye molecule to graphene. J. Chem. Phys. 129, 054703 (2008).
46.Swathi, R.S. and Sebastian, K.L.: Long range resonance energy transfer from a dye molecule to graphene has (distance)−4 dependence. J. Chem. Phys. 130, 086101 (2009).
47.Liu, M., Zhao, H.M., Quan, X., Chen, S., and Fan, X.F.: Distance-independent quenching of quantum dots by nanoscale-graphene in self-assembled sandwich immunoassay. Chem. Commun. 2010, 79097911 (2010).
48.Liu, J.W.: Adsorption of DNA onto gold nanoparticles and graphene oxide: surface science and applications. Phys. Chem. Chem. Phys. 14, 1048510496 (2012).
49.Liu, M., Zhao, H.M., Chen, S., Yu, H.T., and Quan, X.: Salt-controlled assembly of stacked-graphene for capturing fluorescence and its application in chemical genotoxicity screening. J. Mater. Chem. 21, 1526615272 (2011).
50.Mei, S.H., Liu, Z., Brennan, J.D., and Li, Y.: An efficient RNA-cleaving DNA enzyme that synchronizes catalysis with fluorescence signaling. J. Am. Chem. Soc. 125, 412420 (2003).
51.Aguirre, S.D., Ali, M.M., Salena, B.J., and Li, Y.: A sensitive DNA enzyme-based fluorescent assay for bacterial detection. Biomolecules 3, 563577 (2013).
52.Wang, X., Du, Y., Li, Y., Li, D., and Sun, R.: Fluorescent identification and detection of staphylococcus aureus with carboxymethyl chitosan/CdS quantum dots bioconjugates. J. Biomater. Sci., Polym. Ed. 22, 18811893 (2011).
53.Lin, Y.S., Tsai, P.J., Weng, M.F., and Chen, Y.C.: Affinity capture using vancomycin-cound magnetic nanoparticles for the MALDI-MS analysis of bacteria. Anal. Chem. 77, 17531760 (2005).
54.Ji, J., Schanzle, J.A., and Tabacco, M.B.: Real-time detection of bacterial contamination in dynamic aqueous environments using optical sensors. Anal. Chem. 76, 14111418 (2004).
55.Zhao, W., Ali, M.M., Brook, M.A., and Li, Y.: Rolling circle amplification: applications in nanotechnology and biodetection with functional nucleic acids. Angew. Chem. Int. Ed. 47, 63306337 (2008).
56.Ali, M.M., Li, F., Zhang, Z., Zhang, K., Kang, D.K., Ankrum, J.A., Le, X.C., and Zhao, W.: Rolling circle amplification: a versatile tool for chemical biology, materials science and medicine. Chem. Soc. Rev. 43, 33243341 (2014).
57.Liu, M., Zhang, Q., Li, Z., Gu, J., Brennan, J.D., and Li, Y.: Programming a topologically constrained DNA nanostructure into a sensor. Nat. Commun. 7, 12074 (2016).
58.Liu, M., Hui, C.Y., Zhang, Q., Gu, J., Kannan, B., Jahanshahi-Anbuhi, S., Filipe, C.D., Brennan, J.D., and Li, Y.: Target-induced and equipment-free DNA amplification with a simple paper device. Angew. Chem. Int. Ed. 55, 27092713 (2016).
59.Liu, M., Zhang, Q., Gu, J., Brennan, J.D., and Li, Y.: A DNAzyme feedback amplification strategy for biosensing. Angew. Chem. Int. Ed. 56, 61426146 (2017).
60.Liu, M., Yin, Q., McConnell, E.M., Chang, Y., Brennan, J.D., and Li, Y.: DNAzyme feedback amplification: relaying molecular recognition to exponential DNA amplification. Chem. Euro. J. 24, 44734479 (2018).
61.Wang, R., Ruan, C., Kanayeva, D., Lassiter, K., and Li, Y.: TiO2 nanowire bundle microelectrode based impedance immunosensor for rapid and sensitive detection of Listeria monocytogenes. Nano Lett. 8, 26252631 (2008).
62.Labib, M., Zamay, A.S., Kolovskaya, O.S., Reshetneva, I.T., Zamay, G.S., Kibbee, R.J., Sattar, S.A., Zamay, T.N., and Berezovski, M.V.: Aptamer-based viability impedimetric sensor for bacteria. Anal. Chem. 84, 89668969 (2012).
63.Liébana, S., Spricigo, D.A., Cortés, M.P., Barbé, J., Llagostera, M., Alegret, S., and Pividori:, M.I. Phagomagnetic separation and electrochemical magneto-genosensing of pathogenic bacteria. Anal. Chem. 85, 30793086 (2013).
64.Hossain, S.M.Z., Ozimok, C., Sicard, C., Aguirre, S.D., Ali, M.M., Li, Y., and Brennan, J.D.: Multiplexed paper test strip for quantitative bacterial detection. Anal. Bioanal. Chem. 403, 15671576 (2012).
65.Lazcka, O., Del Campo, F.J., and Munoz, F.X.: Pathogen detection: a perspective of traditional methods and biosensors, Biosens. Bioelectron. 22, 12051217 (2007).
66.Postollec, F., Falentin, H., Pavan, S., Combrisson, J., and Sohier, D.: Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiol. 28, 848861 (2011).
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