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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References
Centers for Disease Control and Prevention, CDC Estimates of Foodborne Illness in the United States, Website: http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.htmlfoodborneburden/2011-foodborne-estimates.html.
H. Su, Q. Ma, K. Shang, T. Liu, H. Yin, and S. Ai: Gold nanoparticles as colorimetric sensor: a case study on E. coli O157:H7 as a model for Gram-negative bacteria. Sens. Actuators B. 161, 298–303 (2012).
P. Belgrader, W. Benett, D. Hadley, J. Richards, P. Stratton, R. Mariella, and F. Milanovich: PCR detection of bacteria in seven minutes. Science 284, 449–450 (1999).
D. Ivnitski, I. Abdel-Hamid, P. Atanasov, and E. Wilkins: Flow-through immunofiltration assay system for rapid detection of E. coli O157:H7. Biosens. Bioelectron. 14, 599–624 (1999).
R.M. Jarvis and R. Goodacre: Discrimination of bacteria using surface-enhanced Raman spectroscopy. Anal. Chem. 76, 40–47 (2004).
B.K. Oh, W. Lee, B.S. Chun, Y.M. Bae, W.H. Lee, and J.W. Choi: The fabrication of protein chip based on surface plasmon resonance for detection of pathogens. Biosens. Bioelectron. 20, 1847–1850 (2005).
Z.F. Wang, S. Cheng, S.L. Ge, H. Wang, Q.J. Wang, P.G. He, and Y.Z. Fang: 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, 1687–1694 (2012).
N. Nicolaou, Y. Xu, and R. Goodacre: Detection and quantification of bacterial spoilage in milk and pork meat using MALDI-TOF-MS and multivariate analysis. Anal. Chem. 84, 5951–5958 (2012).
N. Sanvicens, C. Pastells, N. Pascual, and M.P. Marco: Nanoparticle-based biosensors for detection of pathogenic bacteria. Trends Anal. Chem. 28, 1243–1252 (2009).
P.C. Ray, S.A. Khan, A.K. Singh, D. Senapati, and Z. Fan: Nanomaterials for targeted detection and photothermal killing of bacteria. Chem. Soc. Rev. 41, 3193–3209 (2012).
N. Massad-Ivanir, G. Shtenberg, T. Zeidman, and E. Segal: Construction and characterization of porous SiO2/hydrogel hybrids as optical biosensors for rapid detection of bacteria. Adv. Funct. Mater. 20, 2269–2277 (2010).
N. Massad-Ivanir, G. Shtenberg, A. Tzur, M.A. Krepker, and E. Segal: Engineering nanostructured porous SiO2 surfaces for bacteria detection via “direct cell capture”. Anal. Chem. 83, 3282–3289 (2011).
M.A. Hahn, J.S. Tabb, and T.D. Krauss: Detection of single bacterial pathogens with semiconductor quantum dots. Anal. Chem. 77, 4861–4869 (2005).
R. Edgar, M. McKinstry, J. Hwang, A.B. Oppenheim, R.A. Fekete, G. Giulian, C. Merril, K. Nagashima, and S. Adhya: High-sensitivity bacterial detection using biotin-tagged phage and quantum-dot nanocomplexes. Proc. Natl. Acad. Sci. USA 103, 4841–4845 (2006).
C. Wang and J. Irudayaraj: Gold nanorod probes for the detection of multiple pathogens. Small 4, 2204–2208 (2008).
J. Fu, B. Park, and Y. Zhao: Limitation of a localized surface plasmon resonance sensor for Salmonella detection. Sens. Actuators B 141, 276–283 (2009).
A.K. Singh, D. Senapati, S. Wang, J. Griffin, A. Neely, P. Candice, K.M. Naylor, B. Varisli, J.R. Kalluri, and P.C. Ray: Gold nanorod based selective identification of Escherichia coli bacteria using two-photon Rayleigh scattering spectroscopy. ACS Nano 3, 1906–1912 (2009).
X. Xu, Y. Chen, H.J. Wei, B. Xia, F. Liu, and N. Li: Counting bacteria using functionalized gold nanoparticles as the light-scattering reporter. Anal. Chem. 84, 9721–9728 (2012).
W.R. Premasiri, D.T. Moir, M.S. Klempner, N. Krieger, G. Jones, and L.D. Ziegler: Characterization of the surface enhanced Raman scattering (SERS) of bacteria. J. Phys. Chem. B 109, 312–320 (2005).
W.S. Kuo, C.N. Chang, Y.T. Chang, and C.S. Yeh: Antimicrobial gold nanorods with dual-modality photodynamic inactivation and hyperthermia. Chem. Commun. 32, 4853–4855 (2009).
A.J. Kell, G. Stewart, S. Ryan, R. Peytavi, M. Boissinot, A. Huletsky, M. Bergeron, and B. Simard: Vancomycin-modified nanoparticles for efficient targeting and preconcentration of Gram-positive and Gram-negative bacteria. ACS Nano 2, 1777–1788 (2008).
H. Lee, T.J. Yoon, and R. Weissleder: Ultrasensitive detection of bacteria using core-shell nanoparticles and an NMR-filter system. Angew. Chem. Int. Ed. 48, 5657–5660 (2009).
S.P. Ravindranath, L.J. Mauer, C. Deb-Roy, and J. Irudayaraj: Biofunctionalized magnetic nanoparticle integrated mid-infrared pathogen sensor for food matrixes. Anal. Chem. 81, 2840–2846 (2009).
H.J. Chung, T. Reiner, G. Budin, C. Min, M. Liong, D. Issadore, H. Lee, and R. Weissleder: Ubiquitous detection of gram-positive bacteria with bioorthogonal magneto fluorescent nanoparticles. ACS Nano 5, 8834–8841 (2011).
G.A. Zelada-Guillén, J. Riu, A. Düzgün, and F.X. Rius: Immediate detection of living bacteria at ultralow concentrations using a carbon nanotube based potentiometric aptasensor. Angew. Chem., Int. Ed. 48, 7334–7337 (2009).
M.S. Mannoor, H. Tao, J.D. Clayton, A. Sengupta, D.L. Kaplan, R.R. Naik, N. Verma, F.G. Omenetto, and M.C. McAlpine: Graphene-based wireless bacteria detection on tooth enamel. Nat. Commun. 3, 763 (2012).
K.E. Sapsford, W.R. Algar, L. Berti, K.B. Gemmill, B.J. Casey, E. Oh, M.H. Stewart, and I.L. Medintz: Functionalizing nanoparticles with biological molecules: developing chemistries that facilitate nanotechnology. Chem. Rev. 113, 1904–2074 (2013).
W. R. Algar, D.E. Prasuhn, M.H. Stewart, T.L. Jennings, J.B. Blanco-Canosa, P.E. Dawson, and I.L. Medintz: The controlled display of biomolecules on nanoparticles: a challenge suited to bioorthogonal chemistry. Bioconjugate Chem. 22, 825–858 (2011).
T. Soukka, H. Härmä, J. Paukkunen, and T. Lövgren: Utilization of kinetically enhanced monovalent binding affinity by immunoassays based on multivalent nanoparticle-antibody bioconjugates. Anal. Chem. 73, 2254–2260 (2001).
J.A. Mann, T. Alava, H.G. Craighead, and W.R. Dichtel: Preservation of antibody selectivity on graphene by conjugation to a tripod monolayer. Angew. Chem. Int. Ed. 52, 3177–3180 (2013).
L. Chen, X. Zhang, G. Zhou, X. Xiang, X. Ji, Z. Zheng, Z. He, and H. Wang: Simultaneous determination of human enterovirus 71 and coxsackievirus B3 by dual-color quantum dots and homogeneous immunoassay. Anal. Chem. 84, 3200–3207 (2012).
M. Liu, J. Song, S. Shuang, C. Dong, J.D. Brennan, and Y. Li: A graphene-based biosensing platform based on the release of DNA probes and rolling circle amplification. ACS Nano 8, 5564–5573 (2014).
X.H. Zhao, R.M. Kong, X.B. Zhang, H.M. Meng, W.N. Liu, W.H. Tan, G.L. Shen, and R.Q. Yu: Graphene-DNAzyme based biosensor for amplified fluorescence “turn-on” detection of Pb2+ with a high selectivity. Anal. Chem. 83, 5062–5066 (2011).
M.M. Ali, S.D. Aguirre, H. Lazim, and Y. Li: Fluorogenic DNAzyme probes as bacterial indicators. Angew. Chem. Int. Ed. 50, 3751–3754 (2011).
Z. Shen, Z. Wu, D. Chang, W. Zhang, K. Tram, C. Lee, P. Kim, B.J. Salena, and Y. Li: A catalytic DNA activated by a specific strain of bacterial pathogen. Angew. Chem. Int. Ed. 55, 2431–2434 (2016).
S. He, L. Qu, Z. Shen, Y. Tan, M. Zeng, F. Liu, Y. Jiang, and Y. Li: Highly specific recognition of breast tumors by an RNA-cleaving fluorogenic DNAzyme probe. Anal. Chem. 87, 569–577 (2015).
M. Liu, D. Chang, and Y. Li: Discovery and biosensing applications of diverse RNA-cleaving DNAzymes. Acc. Chem. Res. 50, 2273–2283 (2017).
D. Morrison, M. Rothenbroker, and Y. Li: DNAzymes: selected for applications. Small Methods 2, 1700319 (2018).
D. Chen, H. Feng, and J.H. Li: Graphene oxide: preparation, functionalization, and electrochemical applications. Chem. Rev. 112, 6027–6053 (2012).
S.J. Guo and S.J. Dong: Graphene and its derivative-based sensing materials for analytical devices. J. Mater. Chem. 21, 18503–18516 (2011).
L.Y. Feng, L. Wu, and X.G. Qu: New horizons for diagnostics and therapeutic applications of graphene and graphene oxide. Adv. Mater. 25, 168–186 (2013).
N. Varghese, U. Mogera, A. Govindaraj, A. Das, P.K. Maiti, A.K. Sood, and C.N.R. Rao: Binding of DNA nucleobases and nucleosides with graphene. Chem. Phys. Chem. 10, 206–210 (2009).
E. Morales-Narváez, and A. Merkoçi: Graphene oxide as an optical biosensing platform. Adv. Mater. 24, 3298–3308 (2012).
S. Kochmann, T. Hirsch, and O.S. Wolfbeis: Graphenes in chemical sensors and biosensors. Trends Anal. Chem. 39, 87–113 (2012).
R.S. Swathi and K.L. Sebastian: Resonance energy transfer from a dye molecule to graphene. J. Chem. Phys. 129, 054703 (2008).
R.S. Swathi and K.L. Sebastian: Long range resonance energy transfer from a dye molecule to graphene has (distance)−4 dependence. J. Chem. Phys. 130, 086101 (2009).
M. Liu, H.M. Zhao, X. Quan, S. Chen, and X.F. Fan: Distance-independent quenching of quantum dots by nanoscale-graphene in self-assembled sandwich immunoassay. Chem. Commun. 2010, 7909–7911 (2010).
J.W. Liu: Adsorption of DNA onto gold nanoparticles and graphene oxide: surface science and applications. Phys. Chem. Chem. Phys. 14, 10485–10496 (2012).
M. Liu, H.M. Zhao, S. Chen, H.T. Yu, and X. Quan: Salt-controlled assembly of stacked-graphene for capturing fluorescence and its application in chemical genotoxicity screening. J. Mater. Chem. 21, 15266–15272 (2011).
S.H. Mei, Z. Liu, J.D. Brennan, and Y. Li: An efficient RNA-cleaving DNA enzyme that synchronizes catalysis with fluorescence signaling. J. Am. Chem. Soc. 125, 412–420 (2003).
S.D. Aguirre, M.M. Ali, B.J. Salena, and Y. Li: A sensitive DNA enzyme-based fluorescent assay for bacterial detection. Biomolecules 3, 563–577 (2013).
X. Wang, Y. Du, Y. Li, D. Li, and R. Sun: Fluorescent identification and detection of staphylococcus aureus with carboxymethyl chitosan/CdS quantum dots bioconjugates. J. Biomater. Sci., Polym. Ed. 22, 1881–1893 (2011).
Y.S. Lin, P.J. Tsai, M.F. Weng, and Y.C. Chen: Affinity capture using vancomycin-cound magnetic nanoparticles for the MALDI-MS analysis of bacteria. Anal. Chem. 77, 1753–1760 (2005).
J. Ji, J.A. Schanzle, and M.B. Tabacco: Real-time detection of bacterial contamination in dynamic aqueous environments using optical sensors. Anal. Chem. 76, 1411–1418 (2004).
W. Zhao, M.M. Ali, M.A. Brook, and Y. Li: Rolling circle amplification: applications in nanotechnology and biodetection with functional nucleic acids. Angew. Chem. Int. Ed. 47, 6330–6337 (2008).
M.M. Ali, F. Li, Z. Zhang, K. Zhang, D.K. Kang, J.A. Ankrum, X.C. Le, and W. Zhao: Rolling circle amplification: a versatile tool for chemical biology, materials science and medicine. Chem. Soc. Rev. 43, 3324–3341 (2014).
M. Liu, Q. Zhang, Z. Li, J. Gu, J.D. Brennan, and Y. Li: Programming a topologically constrained DNA nanostructure into a sensor. Nat. Commun. 7, 12074 (2016).
M. Liu, C.Y. Hui, Q. Zhang, J. Gu, B. Kannan, S. Jahanshahi-Anbuhi, C.D. Filipe, J.D. Brennan, and Y. Li: Target-induced and equipment-free DNA amplification with a simple paper device. Angew. Chem. Int. Ed. 55, 2709–2713 (2016).
M. Liu, Q. Zhang, J. Gu, J.D. Brennan, and Y. Li: A DNAzyme feedback amplification strategy for biosensing. Angew. Chem. Int. Ed. 56, 6142–6146 (2017).
M. Liu, Q. Yin, E.M. McConnell, Y. Chang, J.D. Brennan, and Y. Li: DNAzyme feedback amplification: relaying molecular recognition to exponential DNA amplification. Chem. Euro. J. 24, 4473–4479 (2018).
R. Wang, C. Ruan, D. Kanayeva, K. Lassiter, and Y. Li: TiO2 nanowire bundle microelectrode based impedance immunosensor for rapid and sensitive detection of Listeria monocytogenes. Nano Lett. 8, 2625–2631 (2008).
M. Labib, A.S. Zamay, O.S. Kolovskaya, I.T. Reshetneva, G.S. Zamay, R.J. Kibbee, S.A. Sattar, T.N. Zamay, and M.V. Berezovski: Aptamer-based viability impedimetric sensor for bacteria. Anal. Chem. 84, 8966–8969 (2012).
S. Liébana, D.A. Spricigo, M.P. Cortés, J. Barbé, M. Llagostera, S. Alegret, and M.I. Pividori: Phagomagnetic separation and electrochemical magneto-genosensing of pathogenic bacteria. Anal. Chem. 85, 3079–3086 (2013).
S.M.Z. Hossain, C. Ozimok, C. Sicard, S.D. Aguirre, M.M. Ali, Y. Li, and J.D. Brennan: Multiplexed paper test strip for quantitative bacterial detection. Anal. Bioanal. Chem. 403, 1567–1576 (2012).
O. Lazcka, F.J. Del Campo, and F.X. Munoz: Pathogen detection: a perspective of traditional methods and biosensors, Biosens. Bioelectron. 22, 1205–1217 (2007).
F. Postollec, H. Falentin, S. Pavan, J. Combrisson, and D. Sohier: Recent advances in quantitative PCR (qPCR) applications in food microbiology. Food Microbiol. 28, 848–861 (2011).
Acknowledgments
Funding for this work was provided by Natural Sciences and Engineering Council of Canada Discovery Grants (J.D.B. and Y.L.), the Canada Foundation for Innovation and the Ontario Ministry for Research and Innovation. Part of the work was conducted at the McMaster Biointerfaces Institute. J.D.B. holds the Canada Research Chair in Bioanalytical Chemistry and Biointerfaces.
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Liu, M., Zhang, Q., Brennan, J.D. et al. Graphene-DNAzyme-based fluorescent biosensor for Escherichia coli detection. MRS Communications 8, 687–694 (2018). https://doi.org/10.1557/mrc.2018.97
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DOI: https://doi.org/10.1557/mrc.2018.97