Biological charge transfer via flickering resonance

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 28, 2014, Pages 10049-10054

  Zhang, Yuqi ^a   Liu, Chaoren ^a   Balaeff, Alexander ^a,d   Skourtis, Spiros S ^b   Beratan, David N ^a,c  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CYPRUS   (Cyprus)

^d UNIVERSITY OF CENTRAL FLORIDA   (United States)

Author keywords

Coherence; Gated transport; Resonant tunneling pathways; Superexchange; Vibronic coupling

Indexed keywords

DNA; NANOWIRE; PORPHYRIN;

ADIABATICITY; ARTICLE; CHARGE TRANSFER; CHEMICAL REACTION KINETICS; CHEMICAL STRUCTURE; DNA HAIRPIN; ELECTRIC ACTIVITY; ELECTRICITY; ELECTRON TRANSPORT; FLICKERING ELECTRONIC RESONANCE; IONIZATION; MACROMOLECULE; PRIORITY JOURNAL; TRANSPORT KINETICS;

COHERENCE; GATED TRANSPORT; RESONANT TUNNELING PATHWAYS; SUPEREXCHANGE; VIBRONIC COUPLING;

BACTERIA; DNA, BACTERIAL; ELECTRON TRANSPORT; KINETICS; MODELS, CHEMICAL; NANOWIRES; OXIDATION-REDUCTION;

EID: 84904325184     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1316519111     Document Type: Article

References (60)

1. Beratan DN, et al. (2009) Steering electrons on moving pathways. Acc Chem Res 42(10):1669-1678.
2. Skourtis SS, Waldeck DH, Beratan DN (2010) Fluctuations in biological and bioinspired electron-transfer reactions. Annu Rev Phys Chem 61:461-485.
3. Skourtis SS (2013) Review: Probing protein electron transfer mechanisms from the molecular to the cellular length scales. Biopolymers 100(1):82-92.
4. Muren NB, Olmon ED, Barton JK (2012) Solution, surface, and single molecule platforms for the study of DNA-mediated charge transport. Phys Chem Chem Phys 14(40):13754-13771.
5. Blankenship RE (2002) Molecular Mechanisms of Photosynthesis (Blackwell Science, Oxford).
6. Susumu K, Frail PR, Angiolillo PJ, Therien MJ (2006) Conjugated chromophore arrays with unusually large hole polaron delocalization lengths. J Am Chem Soc 128(26):8380-8381.
7. El-Naggar MY, et al. (2010) Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci USA 107(42):18127-18131.
8. Malvankar NS, Tuominen MT, Lovley DR (2012) Comment on "on Electrical Conductivity of Microbial Nanowires and Biofilms" by S. M. Strycharz-Glaven, R. M. Snider, A. Guiseppi-Elie and L. M. Tender, Energy Environ Sci, 2011, 4, 4366.
9. Energy Environ Sci 5(3):6247-6249.
10. Mowat CG, Chapman SK (2005) Multi-heme cytochromes - new structures, new chemistry. Dalton Trans (21):3381-3389.
11. Breuer M, Rosso KM, Blumberger J (2014) Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials. Proc Natl Acad Sci USA 111(2):611-616.
12. Stubbe J, Nocera DG, Yee CS, Chang MCY (2003) Radical initiation in the class I ribonucleotide reductase: Long-range proton-coupled electron transfer? Chem Rev 103(6):2167-2201.
13. Shih C, et al. (2008) Tryptophan-accelerated electron flow through proteins. Science 320(5884):1760-1762.
14. Pfeffer C, et al. (2012) Filamentous bacteria transport electrons over centimetre distances. Nature 491(7423):218-221.
15. Gray HB, Winkler JR (2003) Electron tunneling through proteins. Q Rev Biophys 36(3):341-372.
16. Marcus RA, Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811(3):265-322.
17. Hopfield JJ (1974) Electron transfer between biological molecules by thermally activated tunneling. Proc Natl Acad Sci USA 71(9):3640-3644.
18. Ashcroft N, Mermin D (1976) Solid State Physics (W. B. Saunders, Philadelphia).
19. Wolfram Research, Inc (2012) Mathematica (Champaign, IL), Version 9.0.
20. Lewis FD, et al. (2006) Crossover from superexchange to hopping as the mechanism for photoinduced charge transfer in DNA hairpin conjugates. J Am Chem Soc 128(3):791-800.
21. Giese B, Amaudrut J, Köhler A-K, Spormann M, Wessely S (2001) Direct observation of hole transfer through DNA by hopping between adenine bases and by tunnelling. Nature 412(6844):318-320.
22. Grozema FC, et al. (2008) Effect of structural dynamics on charge transfer in DNA hairpins. J Am Chem Soc 130(15):5157-5166.
23. Hatcher E, Balaeff A, Keinan S, Venkatramani R, Beratan DN (2008) PNA versus DNA: Effects of structural fluctuations on electronic structure and hole-transport mechanisms. J Am Chem Soc 130(35):11752-11761.
24. Venkatramani R, Keinan S, Balaeff A, Beratan DN (2011) Nucleic acid charge transfer: Black, white and gray. Coord Chem Rev 255(7-8):635-648.
25. Voityuk AA, Siriwong K, Rösch N (2004) Environmental fluctuations facilitate electron-hole transfer from guanine to adenine in DNA pi stacks. Angew Chem Int Ed Engl 43(5):624-627.
26. Kubar T, Kleinekathöfer U, ElstnerM(2009) Solvent fluctuations drive the hole transfer in DNA: A mixed quantum-classical study. J Phys Chem B 113(39):13107-13117.
27. Beratan D, Skourtis S (1998) Electron transfer mechanisms. Curr Opin Chem Biol 2(2):235-243.
28. Skourtis SS, Beratan DN (1999) Theories of structure-function relationships for bridge-mediated electron transfer reactions. Adv Chem Phys 106:377-452.
29. Kubar T, Elstner M (2008) What governs the charge transfer in DNA? The role of DNA conformation and environment. J Phys Chem B 112(29):8788-8798.
30. Grozema FC, et al. (2009) Effect of GC base pairs on charge transfer through DNA hairpins: The importance of electrostatic interactions. J Am Chem Soc 131(40):14204-14205.
31. Renaud N, Berlin YA, Lewis FD, Ratner MA (2013) Between superexchange and hopping: An intermediate charge-transfer mechanism in poly(A)-poly(T) DNA hairpins. J Am Chem Soc 135(10):3953-3963.
32. Kubař T, Elstner M (2013) Efficient algorithms for the simulation of non-adiabatic electron transfer in complex molecular systems: Application to DNA. Phys Chem Chem Phys 15(16):5794-5813.
33. Kubar T, Elstner M (2009) Solvent reorganization energy of hole transfer in DNA. J Phys Chem B 113(16):5653-5656.
34. Kubar T, Elstner M (2010) Coarse-grained time-dependent density functional simulation of charge transfer in complex systems: Application to hole transfer in DNA. J Phys Chem B 114(34):11221-11240.
35. Voityuk AA (2007) Fluctuation of the electronic coupling in DNA: Multistate versus two-state model. Chem Phys Lett 439(1-3):162-165.
36. Schuster GB, ed (2004) Long-range charge transfer in DNA I and II. Top Curr Chem (Springer, Berlin), Vol 236-237.
37. Berlin YA, Kurnikov IV, Beratan D, Ratner MA, Burin AL (2004) DNA electron transfer processes: Some theoretical notions. Long-range charge transfer in DNA II. Top Curr Chem 237:1-36.
38. Jortner J, Bixon M, Voityuk AA, Rosch N (2002) Superexchange mediated charge hopping in DNA. J Phys Chem A 106(33):7599-7606.
39. Skourtis S, Nitzan A (2003) Effects of initial state preparation on the distance dependence of electron transfer through molecular bridges and wires. J Chem Phys 119(12):6271-6276.
40. Bixon M, Jortner J (2005) Incoherent charge hopping and conduction in DNA and long molecular chains. Chem Phys 319(1-3):273-282.
41. Renger T, Marcus RA (2003) Variable-range hopping electron transfer through disordered bridge states: Application to DNA. J Phys Chem A 107(41):8404-8419.
42. Lewis FD, et al. (2008) Getting to guanine:Mechanism and dynamics of charge separation and charge recombination in DNA revisited. Photochem Photobiol Sci 7(5):534-539.
43. Paul A, et al. (2009) Role of nucleobase energetics and nucleobase interactions in single-stranded peptide nucleic acid charge transfer. J Am Chem Soc 131(18):6498-6507.
44. Venkatramani R, et al. (2011) Evidence for a near-resonant charge transfer mechanism for double-stranded peptide nucleic acid. J Am Chem Soc 133(1):62-72.
45. Voityuk AA (2008) Electronic couplings and on-site energies for hole transfer in DNA: Systematic quantum mechanical/molecular dynamic study. J Chem Phys 128(11):115101.
46. LeBard DN, Lilichenko M, Matyushov DV, Berlin YA, Ratner MA (2003) Solvent reorganization energy of charge transfer in DNA hairpins. J Phys Chem B 107(51):14509-14520.
47. Sugiyama H, Saito I (1996) Theoretical studies of GG-specific photocleavage of DNA via electron transfer: Significant lowering of ionization potential and 5′-localization of HOMO of stacked GG bases in B-form DNA. J Am Chem Soc 118(30):7063-7068.
48. Olofsson J, Larsson S (2001) Electron hole transport in DNA. J Phys Chem B 105(42):10398-10406.
49. Lewis FD, Liu J, Zuo X, Hayes RT, Wasielewski MR (2003) Dynamics and energetics of single-step hole transport in DNA hairpins. J Am Chem Soc 125(16):4850-4861.
50. Bixon M, et al. (1999) Long-range charge hopping in DNA. Proc Natl Acad Sci USA 96(21):11713-11716.
51. Giese B, Spichty M (2000) Long distance charge transport through DNA: Quantification and extension of the hopping model. ChemPhysChem 1(4):195-198.
52. Lewis FD, et al. (2000) Direct measurement of hole transport dynamics in DNA. Nature 406(6791):51-53.
53. Scholes GD (2003) Long-range resonance energy transfer in molecular systems. Annu Rev Phys Chem 54:57-87.
54. Fidler AF, Singh VP, Long PD, Dahlberg PD, Engel GS (2013) Timescales of coherent dynamics in the light harvesting complex 2 (LH2) of Rhodobacter sphaeroides. J Phys Chem Lett 4(9):1404-1409.
55. Fransted KA, Caram JR, Hayes D, Engel GS (2012) Two-dimensional electronic spectroscopy of bacteriochlorophyll a in solution: Elucidating the coherence dynamics of the Fenna-Matthews-Olson complex using its chromophore as a control. J Chem Phys 137(12):125101.
56. Fidler AF, Caram JR, Hayes D, Engel GS (2012) Towards a coherent picture of excitonic coherence in the Fenna-Matthews-Olson complex. J Phys B-At Mol Opt 45(15):154013.
57. Fleming GR, Scholes GD (2004) Physical chemistry: Quantum mechanics for plants. Nature 431(7006):256-257.
58. Wong CY, et al. (2012) Electronic coherence lineshapes reveal hidden excitonic correlations in photosynthetic light harvesting. Nat Chem 4(5):396-404.
59. Schlau-Cohen GS, De Re E, Cogdell RJ, Fleming GR (2012) Determination of excited-state energies and dynamics in the B band of the bacterial reaction center with 2D electronic spectroscopy. J Phys Chem Lett 3(17):2487-2492.
60. Zaks J, Amarnath K, Kramer DM, Niyogi KK, Fleming GR (2012) A kinetic model of rapidly reversible nonphotochemical quenching. Proc Natl Acad Sci USA 109(39):15757-15762.