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Research Article

Two-color spectroscopy of UV excited ssDNA complex with a single-wall nanotube photoluminescence probe: Fast relaxation by nucleobase autoionization mechanism

Tetyana Ignatova1, Alexander Balaeff2, Michael Blades1, Ming Zheng3, Peter Stoeckl4, Slava V. Rotkin5( )
Physics DepartmentLehigh University16 Memorial Dr. E.BethlehemPA18015USA
NanoScience Technology CenterUniversity of Central Florida12424 Research ParkwaySuite 400OrlandoFL32826USA
National Institute of Standards and Technology100 Bureau DriveGaithersburgMD20899USA
Department of Physics & AstronomyUniversity of Rochester206 Bausch & Lomb HallRochesterNY14627USA
Physics DepartmentCenter for Advanced Materials & Nanotechnology and Center for Photonics & NanoelectronicsLehigh University16 Memorial Dr. E.BethlehemPA18015USA
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Abstract

DNA autoionization is a fundamental process wherein ultraviolet (UV)-photoexcited nucleobases dissipate energy by charge transfer to the environment without undergoing chemical damage. Here, single-wall carbon nanotubes (SWNT) are explored as a photoluminescent reporter for the study of the mechanism and rates of DNA autoionization. Two-color photoluminescence spectroscopy allows separate photoexcitation of the DNA and the SWNTs in the UV and visible range, respectively. A strong SWNT photoluminescence quenching is observed when the UV pump is resonant with the DNA absorption, consistent with charge transfer from the excited states of the DNA to the SWNT. Semiempirical calculations of the DNA-SWNT electronic structure, combined with a Green's function theory for charge transfer, show a 20 fs autoionization rate, dominated by hole transfer. Rate-equation analysis of the spectroscopy data confirms that the quenching rate is limited by thermalization of the free charge carriers transferred to the nanotube reservoir. This approach has great potential for monitoring DNA excitation, autoionization, and chemical damage, both in vivo and in vitro.

Keywords

single-wall nanotubeoptical spectroscopytwo-color spectroscopyDNA autoionizationDNA ultraviolet (UV) excitationquantum-mechanical modeling

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References

1

Middleton, C. T.; de La Harpe, K.; Su, C.; Law, Y. K.; Crespo-Hernández, C. E.; Kohler, B. DNA excited-state dynamics: From single bases to the double helix. Annu. Rev. Phys. Chem. 2009, 60, 217-239.
Crossref Google Scholar
2

Adhikary, A.; Malkhasian, A. Y. S.; Collins, S.; Koppen, J.; Becker, D.; Sevilla, M. D. UVA-visible photo-excitation of guanine radical cations produces sugar radicals in DNA and model structures. Nucleic Acids Res. 2005, 33, 5553-5564.
Crossref Google Scholar
3

Crespo-Hernández, C. E.; Cohen, B.; Hare, P. M.; Kohler, B. Ultrafast excited-state dynamics in nucleic acids. Chem. Rev. 2004, 104, 1977-2020.
Crossref Google Scholar
4

Zhang, Y. Y.; Dood, J.; Beckstead, A. A.; Li, X. -B.; Nguyen, K. V.; Burrows, C. J.; Improta, R.; Kohler, B. Photoinduced electron transfer in DNA: Charge shift dynamics between 8-oxo-guanine anion and adenine. J. Phys. Chem. B 2015, 119, 7491-7502.
Crossref Google Scholar
5

Schwalb, N. K.; Temps, F. Ultrafast electronic relaxation in guanosine is promoted by hydrogen bonding with cytidine. J. Am. Chem. Soc. 2007, 129, 9272-9273.
Crossref Google Scholar
6

Crespo-Hernández, C. E.; Arce, R. Photoionization of DNA and RNA bases, nucleosides and nucleotides through a combination of one- and two-photon pathways upon 266 nm nanosecond laser excitation. Photochem. Photobiol. 2002, 76, 259-267.
Crossref
7

Belau, L.; Wilson, K. R.; Leone, S. R.; Ahmed, M. Vacuum-ultraviolet photoionization studies of the microhydration of DNA bases (guanine, cytosine, adenine, and thymine). J. Phys. Chem. A 2007, 111, 7562-7568.
Crossref Google Scholar
8

Gu, J. D.; Leszczynski, J.; Schaefer, H. F. Interactions of electrons with bare and hydrated biomolecules: From nucleic acid bases to DNA segments. Chem. Rev. 2012, 112, 5603-5640.
Crossref Google Scholar
9

Pecourt, J. -M. L.; Peon, J.; Kohler, B. Ultrafast internal conversion of electronically excited RNA and DNA nucleosides in water. J. Am. Chem. Soc. 2000, 122, 9348-9349.
Crossref Google Scholar
10

Wang, C. -R.; Luo, T.; Lu, Q. -B. On the lifetimes and physical nature of incompletely relaxed electrons in liquid water. Phys. Chem. Chem. Phys. 2008, 10, 4463-4470.
Crossref Google Scholar
11

Smyth, M.; Kohano, J. Excess electron localization in solvated DNA bases. Phys. Rev. Lett. 2011, 106, 238108.
Crossref Google Scholar
12

Hong, G. S.; Diao, S.; Antaris, A. L.; Dai, H. J. Carbon nanomaterials for biological imaging and nanomedicinal therapy. Chem. Rev. 2015, 115, 10816-10906.
Crossref Google Scholar
13

Liu, Z.; Tabakman, S.; Welsher, K.; Dai, H. J. Carbon nanotubes in biology and medicine: In vitro and in vivo detection, imaging and drug delivery. Nano Res. 2009, 2, 85-120.
Crossref Google Scholar
14

Heister, E.; Brunner, E. W.; Dieckmann, G. R.; Jurewicz, I.; Dalton, A. B. Are carbon nanotubes a natural solution? Applications in biology and medicine. ACS Appl. Mater. Interfaces 2013, 5, 1870-1891.
Crossref Google Scholar
15

Liu, Z.; Robinson, J. T.; Tabakman, S. M.; Yang, K.; Dai, H. J. Carbon materials for drug delivery & cancer therapy. Materials Today 2011, 14, 316-323.
Crossref Google Scholar
16

Kang, J. W.; Nguyen, F. T.; Lue, N.; Dasari, R. R.; Heller, D. A. Measuring uptake dynamics of multiple identifiable carbon nanotube species via high-speed confocal Raman imaging of live cells. Nano Lett. 2012, 12, 6170-6174.
Crossref Google Scholar
17

Chilek, J. L.; Wang, R. H.; Draper, R. K.; Pantano, P. Use of gel electrophoresis and Raman spectroscopy to characterize the effect of the electronic structure of single-walled carbon nanotubes on cellular uptake. Anal. Chem. 2014, 86, 2882-2887.
Crossref Google Scholar
18

Jain, A.; Homayoun, A.; Bannister, C. W.; Yum, K. Single-walled carbon nanotubes as near-infrared optical biosensors for life sciences and biomedicine. Biotechnol. J. 2015, 10, 447-459.
Crossref Google Scholar
19

Choi, Y.; Moody, I. S.; Sims, P. C.; Hunt, S. R.; Corso, B. L.; Perez, I.; Weiss, G. A.; Collins, P. G. Single-molecule lysozyme dynamics monitored by an electronic circuit. Science 2012, 335, 319-324.
Crossref Google Scholar
20

Martin, C. R.; Kohli, P. The emerging field of nanotube biotechnology. Nat. Rev. Drug Discov. 2003, 2, 29-37.
Crossref Google Scholar
21

Zhou, W. W.; Wang, Y. Y.; Lim, T. -S.; Pham, T.; Jain, D.; Burke, P. J. Detection of single ion channel activity with carbon nanotubes. Sci. Rep. 2015, 5, 9208.
Crossref Google Scholar
22

Budhathoki-Uprety, J.; Jena, P. V.; Roxbury, D.; Heller, D. A. Helical polycarbodiimide cloaking of carbon nanotubes enables inter-nanotube exciton energy transfer modulation. J. Am. Chem. Soc. 2014, 136, 15545-15550.
Crossref Google Scholar
23

Zheng, M.; Jagota, A.; Semke, E. D.; Diner, B. A.; Mclean, R. S.; Lustig, S. R.; Richardson, R. E.; Tassi, N. G. DNA-assisted dispersion and separation of carbon nanotubes. Nat. Mater. 2003, 2, 338-342.
Crossref Google Scholar
24

Strano, M. S.; Zheng, M.; Jagota, A.; Onoa, G. B.; Heller, D. A.; Barone, P. W.; Usrey, M. L. Understanding the nature of the DNA-assisted separation of single-walled carbon nanotubes using fluorescence and Raman spectroscopy. Nano Lett. 2004, 4, 543-550.
Crossref Google Scholar
25

Lu, G.; Maragakis, P.; Kaxiras, E. Carbon nanotube interaction with DNA. Nano Lett. 2005, 5, 897-900.
Crossref Google Scholar
26

Heller, D. A.; Jeng, E. S.; Yeung, T. -K.; Martinez, B. M.; Moll, A. E.; Gastala, J. B.; Strano, M. S. Optical detection of DNA conformational polymorphism on single-walled carbon nanotubes. Science 2006, 311, 508-511.
Crossref Google Scholar
27

Tu, X. M.; Manohar, S.; Jagota, A.; Zheng, M. DNA sequence motifs for structure-specific recognition and separation of carbon nanotubes. Nature 2009, 460, 250-253.
Crossref Google Scholar
28

Khripin, C. Y.; Manohar, S.; Zheng, M.; Jagota, A. Measurement of electrostatic properties of DNA-carbon nanotube hybrids by capillary electrophoresis. J. Phys. Chem. C 2009, 113, 13616-13621.
Crossref Google Scholar
29

Rotkin, S. V. Electronic properties of nonideal nanotube materials: Helical symmetry breaking in DNA hybrids. Annu. Rev. Phys. Chem. 2010, 61, 241-264.
Crossref Google Scholar
30

Roxbury, D.; Mittal, J.; Jagota, A. Molecular-basis of single-walled carbon nanotube recognition by single-stranded DNA. Nano Lett. 2012, 12, 1464-1469.
Crossref Google Scholar
31

Cherukuri, P.; Bachilo, S. M.; Litovsky, S. H.; Weisman, R. B. Near-infrared fluorescence microscopy of single-walled carbon nanotubes in phagocytic cells. J. Am. Chem. Soc. 2004, 126, 15638-15639.
Crossref Google Scholar
32

Mu, B.; Zhang, J. Q.; McNicholas, T. P.; Reuel, N. F.; Kruss, S.; Strano, M. S. Recent advances in molecular recognition based on nanoengineered platforms. Acc. Chem. Res. 2014, 47, 979-988.
Crossref Google Scholar
33

Fabbro, A.; Bosi, S.; Ballerini, L.; Prato, M. Carbon nanotubes: Artificial nanomaterials to engineer single neurons and neuronal networks. ACS Chem. Neurosci. 2012, 3, 611-618.
Crossref Google Scholar
34

Calvaresi, M.; Zerbetto, F. The devil and holy water: Protein and carbon nanotube hybrids. Acc. Chem. Res. 2013, 46, 2454-2463.
Crossref Google Scholar
35

Mundra, R. V.; Wu, X.; Sauer, J.; Dordick, J. S.; Kane, R. S. Nanotubes in biological applications. Curr. Opin. Biotechnol. 2014, 28, 25-32.
Crossref Google Scholar
36

Zheng, M.; Jagota, A.; Strano, M. S.; Santos, A. P.; Barone, P.; Chou, S. G.; Diner, B. A.; Dresselhaus, M. S.; Mclean, R. S.; Onoa, G. B. et al. Structure-based carbon nanotube sorting by sequence-dependent DNA assembly. Science 2003, 302, 1545-1548.
Crossref Google Scholar
37

Lustig, S. R.; Jagota, A.; Khripin, C.; Zheng, M. Theory of structure-based carbon nanotube separations by ion-exchange chromatography of DNA/CNT hybrids. J. Phys. Chem. B 2005, 109, 2559-2566.
Crossref Google Scholar
38

Snyder, S. E.; Rotkin, S. V. Polarization component of cohesion energy in single-wall carbon nanotube-DNA complexes. JETP Lett. 2006, 84, 348-351.
Crossref Google Scholar
39

Alidori, S.; Asqiriba, K.; Londero, P.; Bergkvist, M.; Leona, M.; Scheinberg, D. A.; McDevitt, M. R. Deploying RNA and DNA with functionalized carbon nanotubes. J. Phys. Chem. C 2013, 117, 5982-5992.
Crossref Google Scholar
40

Roxbury, D.; Jagota, A.; Mittal, J. Structural characteristics of oligomeric DNA strands adsorbed onto single-walled carbon nanotubes. J. Phys. Chem. B 2013, 117, 132-140.
Crossref Google Scholar
41

Landry, M. P.; Vukovic, L.; Kruss, S.; Bisker, G.; Landry, A. M.; Islam, S.; Jain, R.; Schulten, K.; Strano, M. S. Comparative dynamics and sequence dependence of DNA and RNA binding to single walled carbon nanotubes. J. Phys. Chem. C 2015, 119, 10048-10058.
Crossref Google Scholar
42

Puller, V. I.; Rotkin, S. V. Helicity and broken symmetry of DNA-nanotube hybrids. EPL 2007, 77, 27006.
Crossref Google Scholar
43

Wall, A.; Ferreira, M. S. Electronic density of states of helically-wrapped carbon nanotubes. J. Phys. : Condens. Matter 2007, 19, 406227.
Crossref Google Scholar
44

Snyder, S. E.; Rotkin, S. V. Optical identification of a DNA-wrapped carbon nanotube: Signs of helically broken symmetry. Small 2008, 4, 1284-1286.
Crossref Google Scholar
45

Hughes, M. E.; Brandin, E.; Golovchenko, J. A. Optical absorption of DNA-carbon nanotube structures. Nano Lett. 2007, 7, 1191-1194.
Crossref Google Scholar
46

Cathcart, H.; Nicolosi, V.; Hughes, J. M.; Blau, W. J.; Kelly, J. M.; Quinn, S. J.; Coleman, J. N. Ordered DNA wrapping switches on luminescence in single-walled nanotube dispersions. J. Am. Chem. Soc. 2008, 130, 12734-12744.
Crossref Google Scholar
47

Duque, J. G.; Pasquali, M.; Cognet, L.; Lounis, B. Environmental and synthesis-dependent luminescence properties of individual single-walled carbon nanotubes. ACS Nano 2009, 3, 2153-2156.
Crossref Google Scholar
48

Fagan, J. A.; Zheng, M.; Rastogi, V.; Simpson, J. R.; Khripin, C. Y.; Silvera Batista, C. A.; Hight Walker, A. R. Analyzing surfactant structures on length and chirality resolved (6, 5) single-wall carbon nanotubes by analytical ultracentrifugation. ACS Nano 2013, 7, 3373-3387.
Crossref Google Scholar
49

Petersen, E. J.; Tu, X. M.; Dizdaroglu, M.; Zheng, M.; Nelson, B. C. Protective roles of single-wall carbon nanotubes in ultrasonication-induced DNA base damage. Small 2013, 9, 205-208.
Crossref Google Scholar
50

Zhang, Y. Q.; Liu, C. R.; Balae, A.; Skourtis, S. S.; Beratan, D. N. Biological charge transfer via flickering resonance. Proc. Natl. Acad. Sci. USA 2014, 111, 10049-10054.
Crossref Google Scholar
51

Giese, B.; Amaudrut, J.; Köhler, A. K.; Spormann, M.; Wessely, S. Direct observation of hole transfer through DNA by hopping between adenine bases and by tunneling. Nature 2001, 412, 318-320.
Crossref Google Scholar
52

Barnett, R. N.; Cleveland, C. L.; Joy, A.; Landman, U.; Schuster, G. B. Charge migration in DNA: Ion-gated transport. Science 2001, 294, 567-571.
Crossref Google Scholar
53

Senthilkumar, K.; Grozema, F. C.; Guerra, C. F.; Bickelhaupt, F. M.; Lewis, F. D.; Berlin, Y. A.; Ratner, M. A.; Siebbeles, L. D. A. Absolute rates of hole transfer in DNA. J. Am. Chem. Soc. 2005, 127, 14894-14903.
Crossref Google Scholar
54

Lewis, F. D.; Wu, T. F.; Zhang, Y. F.; Letsinger, R. L.; Greenfield, S. R.; Wasielewski, M. R. Distance-dependent electron transfer in DNA hairpins. Science 1997, 277, 673-676.
Crossref Google Scholar
55

Genereux, J. C.; Barton, J. K. Mechanisms for DNA charge transport. Chem. Rev. 2010, 110, 1642-1662.
Crossref Google Scholar
56

Lewis, F. D.; Zhu, H. H.; Daublain, P.; Fiebig, T.; Raytchev, M.; Wang, Q.; Shafirovich, V. Crossover from superexchange to hopping as the mechanism for photoinduced charge transfer in DNA hairpin conjugates. J. Am. Chem. Soc. 2006, 128, 791-800.
Crossref Google Scholar
57

Renaud, N.; Berlin, Y. A.; Lewis, F. D.; Ratner, M. A. Between superexchange and hopping: An intermediate charge-transfer mechanism in poly(A)-poly(T) DNA hairpins. J. Am. Chem. Soc. 2013, 135, 3953-3963.
Crossref Google Scholar
58

Dresselhaus, M. S.; Dresselhaus, G.; Avouris, P. Carbon nanotubes: Synthesis, structure, properties, and applications, Vol. 80. In Topics in Applied Physics; Springer: Berlin, Heidelberg, 2001.
Crossref Google Scholar
59

Ajiki, H.; Ando, T. Electronic states of carbon nanotubes. J. Phys. Soc. Jpn. 1993, 62, 1255-1266.
Crossref Google Scholar
60

Ignatova, T.; Najafov, H.; Ryasnyanskiy, A.; Biaggio, I.; Zheng, M.; Rotkin, S. V. Significant FRET between SWNT/DNA and rare earth ions: A signature of their spatial correlations. ACS Nano 2011, 5, 6052-6059.
Crossref Google Scholar
61

Jin, H.; Heller, D. A.; Strano, M. S. Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells. Nano Lett. 2008, 8, 1577-1585.
Crossref Google Scholar
62

Hertel, T.; Himmelein, S.; Ackermann, T.; Stich, D.; Crochet, J. Diffusion limited photoluminescence quantum yields in 1-D semiconductors: Single-wall carbon nanotubes. ACS Nano 2010, 4, 7161-7168.
Crossref Google Scholar
63

Ridley, J.; Zerner, M. An intermediate neglect of differential overlap technique for spectroscopy: Pyrrole and the azines. Theoret. Chim. Acta 1973, 32, 111-134.
Crossref Google Scholar
64

Voityuk, A. A. Intermediate neglect of differential overlap for spectroscopy. WIREs Comput. Mol. Sci. 2013, 3, 515-527.
Crossref Google Scholar
65
Tejerina, B.; Reimers, J. CNDO/INDO. 2014, DOI 10.4231/D3R49G96G. nanoHUB. org. https://nanohub.org/resources/3352 (accessed Sep 3, 2015).
66

Venkatramani, R.; Keinan, S.; Balaeff, A.; Beratan, D. N. Nucleic acid charge transfer: Black, white and gray. Coord. Chem. Rev. 2011, 255, 635-648.
Crossref Google Scholar
67

Venkatramani, R.; Davis, K. L.; Wierzbinski, E.; Bezer, S.; Balaeff, A.; Keinan, S.; Paul, A.; Kocsis, L.; Beratan, D. N.; Achim, C. et al. Evidence for a near-resonant charge transfer mechanism for double-stranded peptide nucleic acid. J. Am. Chem. Soc. 2011, 133, 62-77.
Crossref Google Scholar
68

Hatcher, E.; Balaeff, A.; Keinan, S.; Venkatramani, R.; Beratan, D. N. PNA versus DNA: Effects of structural fluctuations on electronic structure and hole-transport mechanisms. J. Am. Chem. Soc. 2008, 130, 11752-11761.
Crossref Google Scholar
69

Fonseca, A.; Perpète, E. A.; Galet, P.; Champagne, B.; Nagy, J. B.; André, J. M.; Lambin, P.; Lucas, A. A. Quantum chemical evaluation of the knee angle in the (5, 5)-(9, 0) coiled carbon tubule. J. Phys. B: At. Mol. Opt. Phys. 1996, 29, 4915-4924.
Crossref Google Scholar
70

Voityuk, A. A. Fluctuation of the electronic coupling in DNA: Multistate versus two-state model. Chem. Phys. Lett. 2007, 439, 162-165.
Crossref Google Scholar
71

Voityuk, A. A. Electronic couplings and on-site energies for hole transfer in DNA: Systematic quantum mechanical/molecular dynamic study. J. Chem. Phys. 2008, 128, 115101.
Crossref Google Scholar
72

Thiel, W. Semiempirical quantum-chemical methods. WIREs Comput. Mol. Sci. 2014, 4, 145-147.
Crossref Google Scholar
73

Voityuk, A. A. Assessment of semiempirical methods for the computation of charge transfer in DNA π-stacks. Chem. Phys. Lett. 2006, 427, 177-180.
Crossref Google Scholar
74

Kilina, S.; Tretiak, S. Excitonic and vibrational properties of single-walled semiconducting carbon nanotubes. Adv. Funct. Mater. 2007, 17, 3405-3420.
Crossref Google Scholar
75

Chen, H. N.; Ratner, M. A.; Schatz, G. C. Time-dependent theory of the rate of photo-induced electron transfer. J. Phys. Chem. C 2011, 115, 18810-18821.
Crossref Google Scholar
76

Santoro, F.; Improta, R.; Avila, F.; Segado, M.; Lami, A. The interplay between neutral exciton and charge transfer states in single-strand polyadenine: A quantum dynamical investigation. Photochem. Photobiol. Sci. 2013, 12, 1527-1543.
Crossref Google Scholar
77

Tataurov, A. V.; You, Y.; Owczarzy, R. Predicting ultraviolet spectrum of single stranded and double stranded deoxyribonucleic acids. Biophys. Chem. 2008, 133, 66-70.
Crossref Google Scholar
Nano Research
Volume 9 Issue 2,
February 2016
Pages 571-583
DOI: 10.1007/s12274-015-0938-0
Cite this article:
Ignatova T, Balaeff A, Blades M, et al. Two-color spectroscopy of UV excited ssDNA complex with a single-wall nanotube photoluminescence probe: Fast relaxation by nucleobase autoionization mechanism. Nano Research, 2016, 9(2): 571-583. https://doi.org/10.1007/s12274-015-0938-0

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Received: 03 September 2015
Accepted: 04 November 2015
Published: 13 January 2016
© Tsinghua University Press and Springer-Verlag Berlin Heidelberg 2015
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