1932

Abstract

The corpus of electron transfer (ET) theory provides considerable power to describe the kinetics and dynamics of electron flow at the nanoscale. How is it, then, that nucleic acid (NA) ET continues to surprise, while protein-mediated ET is relatively free of mechanistic bombshells? I suggest that this difference originates in the distinct electronic energy landscapes for the two classes of reactions. In proteins, the donor/acceptor-to-bridge energy gap is typically several-fold larger than in NAs. NA ET can access tunneling, hopping, and resonant transport among the bases, and fluctuations can enable switching among mechanisms; protein ET is restricted to tunneling among redox active cofactors and, under strongly oxidizing conditions, a few privileged amino acid side chains. This review aims to provide conceptual unity to DNA and protein ET reaction mechanisms. The establishment of a unified mechanistic framework enabled the successful design of NA experiments that switch electronic coherence effects on and off for ET processes on a length scale of multiple nanometers and promises to provide inroads to directing and detecting charge flow in soft-wet matter.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-physchem-042018-052353
2019-06-14
2024-04-15
Loading full text...

Full text loading...

/deliver/fulltext/physchem/70/1/annurev-physchem-042018-052353.html?itemId=/content/journals/10.1146/annurev-physchem-042018-052353&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Bertini I, Gray HB, Stiefel EI, Valentine JS 2007. Biological Inorganic Chemistry: Structure and Reactivity Mill Valley, CA: Univ. Sci. Books
  2. 2.
    Phillips R, Kondev J, Theriot J, Garcia H 2013. Physical Biology of the Cell New York: Garland Sci, 2nd ed..
  3. 3.
    Marcus RA 1993. Electron-transfer reactions in chemistry—theory and experiment. Rev. Mod. Phys. 65:599–610
    [Google Scholar]
  4. 4.
    Marcus RA, Sutin N 1985. Electron transfers in chemistry and biology. Biochim. Biophys. Acta 811:265–322
    [Google Scholar]
  5. 5.
    Balzani V 2001. Electron Transfer in Chemistry Vol. 1–5 Weinheim, Ger: Wiley-VCH
  6. 6.
    Beratan DN, Skourtis SS, Balabin IA, Balaeff A, Keinan S et al. 2009. Steering electrons on moving pathways. Acc. Chem. Res. 42:1669–78
    [Google Scholar]
  7. 7.
    Beratan DN, Liu CR, Migliore A, Polizzi NF, Skourtis SS et al. 2015. Charge transfer in dynamical biosystems, or the treachery of (static) images. Acc. Chem. Res. 48:474–81This recent review describes the FR model and the role of fluctuations in biological ET.
    [Google Scholar]
  8. 8.
    Skourtis SS, Beratan DN 1999. Theories of structure-function relationships for bridge-mediated electron transfer reactions. Adv. Chem. Phys. 106:377–452
    [Google Scholar]
  9. 9.
    Hopfield JJ 1974. Electron transfer between biological molecules by thermally activated tunneling. PNAS 71:3640–44
    [Google Scholar]
  10. 10.
    Beratan DN, Betts JN, Onuchic JN 1991. Protein electron transfer rates set by the bridging secondary and tertiary structure. Science 252:1285–88
    [Google Scholar]
  11. 11.
    Beratan DN, Onuchic JN, Hopfield JJ 1987. Electron-tunneling through covalent and noncovalent pathways in proteins. J. Chem. Phys. 86:4488–98
    [Google Scholar]
  12. 12.
    Venkatramani R, Keinan S, Balaeff A, Beratan DN 2011. Nucleic acid charge transfer: black, white and gray. Coord. Chem. Rev. 255:635–48This recent review of DNA ET theory, modeling, and simulation emphasizes the role of fluctuations and near-resonant processes.
    [Google Scholar]
  13. 13.
    Schuster GB 2000. Long-range charge transfer in DNA: transient structural distortions control the distance dependence. Acc. Chem. Res. 33:253–60
    [Google Scholar]
  14. 14.
    Murphy CJ, Arkin MR, Jenkins Y, Ghatlia ND, Bossmann SH et al. 1993. Long-range photoinduced electron-transfer through a DNA helix. Science 262:1025–29
    [Google Scholar]
  15. 15.
    Baum R 1993. DNA double helix acts as ‘molecular wire. .’ Chem. Eng. News 71:52–53
    [Google Scholar]
  16. 16.
    Priyadarshy S, Risser SM, Beratan DN 1996. DNA is not a molecular wire: protein-like electron-transfer predicted for an extended π-electron system. J. Phys. Chem. 100:17678–82
    [Google Scholar]
  17. 17.
    Stemp ED, Barton JK 1996. Electron transfer between metal complexes bound to DNA: Is DNA a wire?. Met. Ions Biol. Syst. 33:325–65
    [Google Scholar]
  18. 18.
    Lincoln P, Tuite E, Nordén B 1997. Short-circuiting the molecular wire: cooperative binding of Δ-[Ru(phen)2dppz]2+ and Δ-[Rh(phi)2bipy]3+ to DNA. J. Am. Chem. Soc. 119:1454–55
    [Google Scholar]
  19. 19.
    Diederichsen U 1997. Charge transfer in DNA: a controversy. Angew. Chem. Int. Ed. 36:2317–19
    [Google Scholar]
  20. 20.
    Taubes G 1997. Double helix does chemistry at a distance—but how. ? Science 275:20–21
    [Google Scholar]
  21. 21.
    Wilson EK 1999. DNA conductance convergence? New mechanisms claim to resolve much of the debate over how charge migrates through DNA—but questions remain. Chem. Eng. News 77:43–48
    [Google Scholar]
  22. 22.
    Wilson EK 2001. DNA charge migration: no longer an issue. Chem. Eng. News 79:29
    [Google Scholar]
  23. 23.
    Zwang TJ, Tse ECM, Barton JK 2018. Sensing DNA through DNA charge transport. ACS Chem. Biol. 13:1799–809
    [Google Scholar]
  24. 24.
    Teo RD, Rousseau BJG, Smithwick ER, Di Felice R, Beratan DN, Migliore A 2019. Charge transfer between [4Fe4S] proteins and DNA is unidirectional. Implications for biomolecular signaling. Chem 5:122–37This theoretical study describes key thermodynamic constraints on ET signaling through DNA that may be associated with damage sensing.
    [Google Scholar]
  25. 25.
    Jones MR, Seeman NC, Mirkin CA 2015. Programmable materials and the nature of the DNA bond. Science 347:1260901
    [Google Scholar]
  26. 26.
    O'Brien E, Holt ME, Thompson MK, Salay LE, Ehlinger AC et al. 2017. The [4Fe4S] cluster of human DNA primase functions as a redox switch using DNA charge transport. Science 355:eaag1789
    [Google Scholar]
  27. 27.
    Sontz PA, Muren NB, Barton JK 2012. DNA charge transport for sensing and signaling. Acc. Chem. Res. 45:1792–800
    [Google Scholar]
  28. 28.
    Teo RD, Smithwick ER, Migliore A, Beratan DN 2019. A single AT-GC exchange can modulate charge transfer-induced p53-DNA dissociation. Chem. Commun. 55:206–9
    [Google Scholar]
  29. 29.
    Migliore A, Naaman R, Beratan DN 2015. Sensing of molecules using quantum dynamics. PNAS 112:E2419–28
    [Google Scholar]
  30. 30.
    Lewis FD, Young RM, Wasielewski MR 2018. Tracking photoinduced charge separation in DNA: from start to finish. Acc. Chem. Res. 51:1746–54
    [Google Scholar]
  31. 31.
    Schrödinger E 1944. What Is Life? The Physical Aspect of the Living Cell and Mind Cambridge, UK: Cambridge Univ. Press
  32. 32.
    Longuet-Higgins HC 1962. Quantum mechanics and biology. Biophys. J. 2:207–15
    [Google Scholar]
  33. 33.
    Hopfield JJ 2014. Whatever happened to solid state physics?. Annu. Rev. Condens. Matter Phys. 5:1–13
    [Google Scholar]
  34. 34.
    Polizzi NF, Beratan DN 2015. Open-access, interactive explorations for teaching and learning quantum dynamics. J. Chem. Educ. 92:2161–64
    [Google Scholar]
  35. 35.
    Fleming GR, Scholes GD, De Wit A, eds. 2011. 22nd Solvay conference on chemistry: quantum effects in chemistry and biology. Procedia Chem 3:1–366
    [Google Scholar]
  36. 36.
    Scholes GD, Fleming GR, Chen LX, Aspuru-Guzik A, Buchleitner A et al. 2017. Using coherence to enhance function in chemical and biophysical systems. Nature 543:647–-56This broad recent survey focuses on investigations of coherence effects in molecular and biophysics processes, including conceptual and experimental issues.
    [Google Scholar]
  37. 37.
    Mohseni M, Omar Y, Engel GS, Plenio MB, eds. 2014. Quantum Effects in Biology Cambridge, UK: Cambridge Univ. Press
  38. 38.
    Cramer WA, Knaff DB 1990. Energy Transduction in Biological Membranes: A Textbook of Bioenergetics New York: Springer-Verlag
  39. 39.
    Aquino AJA, Beroza P, Beratan DN, Onuchic JN 1995. Docking and electron-transfer between cytochrome c2 and the photosynthetic reaction-center. Chem. Phys. 197:277–88
    [Google Scholar]
  40. 40.
    Gray HB, Winkler JR 2003. Electron tunneling through proteins. Q. Rev. Biophys. 36:341–72
    [Google Scholar]
  41. 41.
    Pfeffer C, Larsen S, Song J, Dong MD, Besenbacher F et al. 2012. Filamentous bacteria transport electrons over centimetre distances. Nature 491:218–21
    [Google Scholar]
  42. 42.
    Skourtis SS, Balabin IA, Kawatsu T, Beratan DN 2005. Protein dynamics and electron transfer: electronic decoherence and non-condon effects. PNAS 102:3552–57
    [Google Scholar]
  43. 43.
    El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G et al. 2010. Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. PNAS 107:18127–31
    [Google Scholar]
  44. 44.
    Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR 2005. Extracellular electron transfer via microbial nanowires. Nature 435:1098–101
    [Google Scholar]
  45. 45.
    Polizzi NF, Skourtis SS, Beratan DN 2012. Physical constraints on charge transport through bacterial nanowires. Faraday Discuss 155:43–62
    [Google Scholar]
  46. 46.
    Blumberger J 2015. Recent advances in the theory and molecular simulation of biological electron transfer reactions. Chem. Rev. 115:11191–238
    [Google Scholar]
  47. 47.
    Pirbadian S, El-Naggar MY 2012. Multistep hopping and extracellular charge transfer in microbial redox chains. Phys. Chem. Chem. Phys. 14:13802–8
    [Google Scholar]
  48. 48.
    Strycharz-Glaven SM, Snider RM, Guiseppi-Elie A, Tender LM 2011. On the electrical conductivity of microbial nanowires and biofilms. Energ. Environ. Sci. 4:4366–79
    [Google Scholar]
  49. 49.
    Xu S, Jangir Y, El-Naggar MY 2016. Disentangling the roles of free and cytochrome-bound flavins in extracellular electron transport from Shewanella oneidensis MR-1. Electrochim. Acta 198:49–55
    [Google Scholar]
  50. 50.
    Conrado RJ, Haynes CA, Haendler BE, Toone EJ 2013. Electrofuels: a new paradigm for renewable fuels. Advanced Biofuels and Bioproducts JW Lee 1037–64 New York: Springer
    [Google Scholar]
  51. 51.
    Genereux JC, Barton JK 2010. Mechanisms for DNA charge transport. Chem. Rev. 110:1642–62This comprehensive review discusses experimental and conceptual aspects of DNA ET.
    [Google Scholar]
  52. 52.
    Arnold AR, Grodick MA, Barton JK 2016. DNA charge transport: from chemical principles to the cell. Cell Chem. Biol. 23:183–97This review of DNA ET mechanisms includes links to cellular processes.
    [Google Scholar]
  53. 53.
    Murphy CJ, Arkin MR, Jenkins Y, Ghatlia ND, Bossmann SH et al. 1993. Long-range photoinduced electron transfer through a DNA helix. Science 262:1025–29
    [Google Scholar]
  54. 54.
    Priyadarshy S, Risser SM, Beratan DN 1996. DNA is not a molecular wire: protein-like electron-transfer predicted for an extended π-electron system. J. Phys. Chem. 100:17678–82
    [Google Scholar]
  55. 55.
    Beratan DN, Priyadarshy S, Risser SM 1997. DNA: Insulator or wire. ? Chem. Biol. 4:3–8
    [Google Scholar]
  56. 56.
    Felts AK, Pollard WT, Friesner RA 1995. Multilevel redfield treatment of bridge-mediated long-range electron-transfer—a mechanism for anomalous distance dependence. J. Phys. Chem. 99:2929–40
    [Google Scholar]
  57. 57.
    Wan CZ, Fiebig T, Kelley SO, Treadway CR, Barton JK, Zewail AH 1999. Femtosecond dynamics of DNA-mediated electron transfer. PNAS 96:6014–19
    [Google Scholar]
  58. 58.
    Wan CZ, Fiebig T, Schiemann O, Barton JK, Zewail AH 2000. Femtosecond direct observation of charge transfer between bases in DNA. PNAS 97:14052–55
    [Google Scholar]
  59. 59.
    Lewis FD, Liu JQ, Weigel W, Rettig W, Kurnikov IV, Beratan DN 2002. Donor-bridge-acceptor energetics determine the distance dependence of electron tunneling in DNA. PNAS 99:12536–41
    [Google Scholar]
  60. 60.
    Giese B 2002. Long-distance electron transfer through DNA. Annu. Rev. Biochem. 71:51–70
    [Google Scholar]
  61. 61.
    Beall E, Ulku S, Liu C, Wierzbinski E, Zhang Y et al. 2017. Effects of the backbone and chemical linker on the molecular conductance of nucleic acid duplexes. J. Am. Chem. Soc. 139:6726–35
    [Google Scholar]
  62. 62.
    Giese B 2000. Long-distance charge transport in DNA: the hopping mechanism. Acc. Chem. Res. 33:631–36
    [Google Scholar]
  63. 63.
    Lewis FD, Letsinger RL, Wasielewski MR 2001. Dynamics of photoinduced charge transfer and hole transport in synthetic DNA hairpins. Acc. Chem. Res. 34:159–70
    [Google Scholar]
  64. 64.
    Bixon M, Jortner J 2005. Incoherent charge hopping and conduction in DNA and long molecular chains. Chem. Phys. 319:273–82
    [Google Scholar]
  65. 65.
    Bixon M, Giese B, Wessely S, Langenbacher T, Michel-Beyerle ME, Jortner J 1999. Long-range charge hopping in DNA. PNAS 96:11713–16
    [Google Scholar]
  66. 66.
    Bixon M, Jortner J 2002. Long-range and very long-range charge transport in DNA. Chem. Phys. 281:393–408
    [Google Scholar]
  67. 67.
    Renger T, Marcus RA 2003. Variable-range hopping electron transfer through disordered bridge states: application to DNA. J. Phys. Chem. A 107:8404–19
    [Google Scholar]
  68. 68.
    Conwell EM, Rakhmanova SV 2000. Polarons in DNA. PNAS 97:4556–60
    [Google Scholar]
  69. 69.
    Kurnikov IV, Tong GSM, Madrid M, Beratan DN 2002. Hole size and energetics in double helical DNA: competition between quantum delocalization and solvation localization. J. Phys. Chem. B 106:7–10
    [Google Scholar]
  70. 70.
    Lewis FD, Wu T, Zhang Y, Letsinger RL, Greenfield SR, Wasielewski MR 1997. Distance-dependent electron transfer in DNA hairpins. Science 277:673–76The first report of charge transfer in a DNA hairpin structure capped by a stilbene photooxidant shows exponential distance dependence of the rates.
    [Google Scholar]
  71. 71.
    Lewis FD, Wasielewski MR 2013. Dynamics and efficiency of photoinduced charge transport in DNA: toward the elusive molecular wire. Pure Appl. Chem. 85:1379–87
    [Google Scholar]
  72. 72.
    Paul A, Watson RM, Wierzbinski E, Davis KL, Sha A et al. 2010. Distance dependence of the charge transfer rate for peptide nucleic acid monolayers. J. Phys. Chem. B 114:14140–48
    [Google Scholar]
  73. 73.
    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. 119:6271–76
    [Google Scholar]
  74. 74.
    Levine AD, Iv M, Peskin U 2016. Length-independent transport rates in biomolecules by quantum mechanical unfurling. Chem. Sci. 7:1535–42
    [Google Scholar]
  75. 75.
    Lewis FD, Zhu HH, Daublain P, Fiebig T, Raytchev M et al. 2006. Crossover from superexchange to hopping as the mechanism for photoinduced charge transfer in DNA hairpin conjugates. J. Am. Chem. Soc. 128:791–800This report describes the carrier population on the ET bridge in the same systems that display exponential distance dependence.
    [Google Scholar]
  76. 76.
    Zhang YQ, Liu CR, Balaeff A, Skourtis SS, Beratan DN 2014. Biological charge transfer via flickering resonance. PNAS 111:10049–54This article describes the FR model and its application to DNA charge transport.
    [Google Scholar]
  77. 77.
    Onuchic JN, Beratan DN 1987. Molecular bridge effects on distant charge tunneling. J. Am. Chem. Soc. 109:6771–78
    [Google Scholar]
  78. 78.
    Beratan DN, Hopfield JJ 1984. Calculation of electron-tunneling matrix-elements in rigid systems—mixed-valence dithiaspirocyclobutane molecules. J. Am. Chem. Soc. 106:1584–94
    [Google Scholar]
  79. 79.
    Onuchic JN, Beratan DN 1990. A predictive theoretical model for electron tunneling pathways in proteins. J. Chem. Phys. 92:722–33
    [Google Scholar]
  80. 80.
    Onuchic JN, Beratan DN, Winkler JR, Gray HB 1992. Pathway analysis of protein electron-transfer reactions. Annu. Rev. Biophys. Biomol. Struct. 21:349–77
    [Google Scholar]
  81. 81.
    Migliore A, Polizzi NF, Therien MJ, Beratan DN 2014. Biochemistry and theory of proton-coupled electron transfer. Chem. Rev. 114:3381–465
    [Google Scholar]
  82. 82.
    Jiang N, Kuznetsov A, Nocek JM, Hoffman BM, Crane BR et al. 2013. Distance-independent charge recombination kinetics in cytochrome c–cytochrome c peroxidase complexes: compensating changes in the electronic coupling and reorganization energies. J. Phys. Chem. B 117:9129–41
    [Google Scholar]
  83. 83.
    Wolfgang J, Risser SM, Priyadarshy S, Beratan DN 1997. Secondary structure conformations and long range electronic interactions in oligopeptides. J. Phys. Chem. B 101:2986–91
    [Google Scholar]
  84. 84.
    Curry WB, Grabe MD, Kurnikov IV, Skourtis SS, Beratan DN et al. 1995. Pathways, pathway tubes, pathway docking, and propagators in electron-transfer proteins. J. Bioenerg. Biomembr. 27:285–93
    [Google Scholar]
  85. 85.
    Balabin IA, Onuchic JN 2000. Dynamically controlled protein tunneling paths in photosynthetic reaction centers. Science 290:114–17
    [Google Scholar]
  86. 86.
    Prytkova TR, Kurnikov IV, Beratan DN 2005. Ab initio based calculations of electron-transfer rates in metalloproteins. J. Phys. Chem. B 109:1618–25
    [Google Scholar]
  87. 87.
    Prytkova TR, Kurnikov IV, Beratan DN 2007. Coupling coherence distinguishes structure sensitivity in protein electron transfer. Science 315:622–25
    [Google Scholar]
  88. 88.
    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. 130:11752–61This paper describes the fluctuation-induced interchange of adenine and guanine HOMO positions based on quantum-classical simulations.
    [Google Scholar]
  89. 89.
    Tong GSM, Kurnikov IV, Beratan DN 2002. Tunneling energy effects on GC oxidation in DNA. J. Phys. Chem. B 106:2381–92
    [Google Scholar]
  90. 90.
    Balabin IA, Beratan DN, Skourtis SS 2008. Persistence of structure over fluctuations in biological electron-transfer reactions. Phys. Rev. Lett. 101:158102
    [Google Scholar]
  91. 91.
    Skourtis SS 2013. Probing protein electron transfer mechanisms from the molecular to the cellular length scales. Biopolymers 100:82–92
    [Google Scholar]
  92. 92.
    Davidson VL 2000. What controls the rates of interprotein electron-transfer reactions. Acc. Chem. Res. 33:87–93
    [Google Scholar]
  93. 93.
    Davidson VL 2008. Protein control of true, gated, and coupled electron transfer reactions. Acc. Chem. Res. 41:730–38
    [Google Scholar]
  94. 94.
    Skourtis SS, Waldeck DH, Beratan DN 2010. Fluctuations in biological and bioinspired electron-transfer reactions. Annu. Rev. Phys. Chem. 61:461–85This comprehensive review describes the fluctuation processes and timescales that enter ET reactions.
    [Google Scholar]
  95. 95.
    Skourtis SS, Lin J, Beratan DN 2006. The effects of bridge motion on electron transfer reactions mediated by tunneling. Modern Methods for Theoretical Physical Chemistry of Biopolymers EB Starikov, JP Lewis, S Tanaka 357–82 Boston: Elsevier
    [Google Scholar]
  96. 96.
    Yue H, Khoshtariya D, Waldeck DH, Grochol J, Hildebrandt P, Murgida DH 2006. On the electron transfer mechanism between cytochrome c and metal electrodes. Evidence for dynamic control at short distances. J. Phys. Chem. B 110:19906–13
    [Google Scholar]
  97. 97.
    Beratan DN, Onuchic JN 1988. Adiabaticity and nonadiabaticity in bimolecular outer-sphere charge-transfer reactions. J. Chem. Phys. 89:6195–203
    [Google Scholar]
  98. 98.
    Skourtis SS, Dasilva AJR, Bialek W, Onuchic JN 1992. A new look at the primary charge separation in bacterial photosynthesis. J. Phys. Chem. 96:8034–41
    [Google Scholar]
  99. 99.
    Subotnik JE, Jain A, Landry B, Petit A, Ouyang WJ, Bellonzi N 2016. Understanding the surface hopping view of electronic transitions and decoherence. Annu. Rev. Phys. Chem. 67:387–417
    [Google Scholar]
  100. 100.
    Woiczikowski PB, Steinbrecher T, Kubar T, Elstner M 2011. Nonadiabatic QM/MM simulations of fast charge transfer in Escherichia coli DNA photolyase. J. Phys. Chem. B 115:9846–63
    [Google Scholar]
  101. 101.
    Renaud N, Harris MA, Singh APN, Berlin YA, Ratner MA et al. 2016. Deep-hole transfer leads to ultrafast charge migration in DNA hairpins. Nat. Chem. 8:1015–21
    [Google Scholar]
  102. 102.
    Gray HB, Winkler JR 2015. Hole hopping through tyrosine/tryptophan chains protects proteins from oxidative damage. PNAS 112:10920–25
    [Google Scholar]
  103. 103.
    Winkler JR, Gray HB 2015. Electron flow through biological molecules: Does hole hopping protect proteins from oxidative damage?. Q. Rev. Biophys. 48:411–20
    [Google Scholar]
  104. 104.
    Polizzi NF, Migliore A, Therien MJ, Beratan DN 2015. Defusing redox bombs. ? PNAS 112:10821–22
    [Google Scholar]
  105. 105.
    Beratan DN, Waldeck DH 2016. Hot holes break the speed limit. Nat. Chem. 8:992–93
    [Google Scholar]
  106. 106.
    Peters JW, Beratan DN, Schut GJ, Adams MWW 2018. On the nature of organic and inorganic centers that bifurcate electrons, coupling exergonic and endergonic oxidation-reduction reactions. Chem. Commun. 54:4091–99
    [Google Scholar]
  107. 107.
    Zhang P, Yuly JL, Lubner CE, Mulder DW, King PW et al. 2017. Electron bifurcation: thermodynamics and kinetics of two-electron brokering in biological redox chemistry. Acc. Chem. Res. 50:2410–17This paper describes electron bifurcation processes in the context of modern ET theory.
    [Google Scholar]
  108. 108.
    Weiss EA, Ahrens MJ, Sinks LE, Gusev AV, Ratner MA, Wasielewski MR 2004. Making a molecular wire: charge and spin transport through para-phenylene oligomers. J. Am. Chem. Soc. 126:5577–84
    [Google Scholar]
  109. 109.
    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 GB Schuster 1–36 Top. Curr. Chem. 237 Berlin: Springer
    [Google Scholar]
  110. 110.
    Kubar T, Elstner M 2008. What governs the charge transfer in DNA? The role of DNA conformation and environment. J. Phys. Chem. B 112:8788–98
    [Google Scholar]
  111. 111.
    Gutierrez R, Caetano R, Woiczikowski PB, Kubar T, Elstner M, Cuniberti G 2010. Structural fluctuations and quantum transport through DNA molecular wires: a combined molecular dynamics and model Hamiltonian approach. New J. Phys. 12:023022
    [Google Scholar]
  112. 112.
    Cailliez F, Muller P, Firmino T, Pernot P, de la Lande A 2016. Energetics of photoinduced charge migration within the tryptophan tetrad of an animal (6–4) photolyase. J. Am. Chem. Soc. 138:1904–15
    [Google Scholar]
  113. 113.
    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. 135:3953–63
    [Google Scholar]
  114. 114.
    Levine AD, Iv M, Peskin U 2018. Formulation of long-range transport rates through molecular bridges: from unfurling to hopping. J. Phys. Chem. Lett. 9:4139–45
    [Google Scholar]
  115. 115.
    Kim H, Segal D 2017. Controlling charge transport mechanisms in molecular junctions: distilling thermally induced hopping from coherent-resonant conduction. J. Chem. Phys. 146:164702
    [Google Scholar]
  116. 116.
    Venkatramani R, Davis KL, Wierzbinski E, Bezer S, Balaeff A et al. 2011. Evidence for a near-resonant charge transfer mechanism for double-stranded peptide nucleic acid. J. Am. Chem. Soc. 133:62–72
    [Google Scholar]
  117. 117.
    Venkatramani R, Wierzbinski E, Waldeck DH, Beratan DN 2014. Breaking the simple proportionality between molecular conductances and charge transfer rates. Faraday Discuss 174:57–78
    [Google Scholar]
  118. 118.
    Wierzbinski E, Venkatramani R, Davis KL, Bezer S, Kong J et al. 2013. The single-molecule conductance and electrochemical electron-transfer rate are related by a power law. ACS Nano 7:5391–401
    [Google Scholar]
  119. 119.
    Xing YJ, Park TH, Venkatramani R, Keinan S, Beratan DN et al. 2010. Optimizing single-molecule conductivity of conjugated organic oligomers with carbodithioate linkers. J. Am. Chem. Soc. 132:7946–56
    [Google Scholar]
  120. 120.
    Xiang LM, Palma JL, Bruot C, Mujica V, Ratner MA, Tao NJ 2015. Intermediate tunnelling-hopping regime in DNA charge transport. Nat. Chem. 7:221–26This paper describes experimental break-junction studies on DNA G-blocks that display resistance oscillations characteristic of electronic coherence.
    [Google Scholar]
  121. 121.
    Liu CR, Xiang LM, Zhang YQ, Zhang P, Beratan DN et al. 2016. Engineering nanometre-scale coherence in soft matter. Nat. Chem. 8:941–45This article reports on theoretical designs and experimental validations of coherence engineering in nanometer-scale DNA constructs through exploiting FR mechanisms.
    [Google Scholar]
  122. 122.
    Liu CR, Beratan DN, Zhang P 2016. Coarse-grained theory of biological charge transfer with spatially and temporally correlated noise. J. Phys. Chem. B 120:3624–33
    [Google Scholar]
  123. 123.
    Young RM, Singh APN, Thazhathveetil AK, Cho VY, Zhang YQ et al. 2015. Charge transport across DNA-based three-way junctions. J. Am. Chem. Soc. 137:5113–22
    [Google Scholar]
  124. 124.
    Sha RJ, Xiang LM, Liu CR, Balaeff A, Zhang YQ et al. 2018. Charge splitters and charge transport junctions based on guanine quadruplexes. Nat. Nanotechnol. 13:316–21This paper describes the simulation and experimental characterization of a current splitter based on a DNA G4 box motif
    [Google Scholar]
  125. 125.
    Zhang YQ, Zhang WB, Liu CR, Zhang P, Balaeff A, Beratan DN 2016. DNA charge transport: moving beyond 1D. Surf. Sci. 652:33–38
    [Google Scholar]
  126. 126.
    Zhang YQ, Young RM, Thazhathveetil AK, Singh APN, Liu CR et al. 2015. Conformationally gated charge transfer in DNA three-way junctions. J. Phys. Chem. Lett. 6:2434–38
    [Google Scholar]
  127. 127.
    Mondal PC, Fontanesi C, Waldeck DH, Naaman R 2016. Spin-dependent transport through chiral molecules studied by spin-dependent electrochemistry. Acc. Chem. Res. 49:2560–68
    [Google Scholar]
  128. 128.
    Naaman R, Waldeck DH 2015. Spintronics and chirality: spin selectivity in electron transport through chiral molecules. Annu. Rev. Phys. Chem. 66:263–81This paper describes spin filtering in chiral structures, including DNA.
    [Google Scholar]
  129. 129.
    Michaeli K, Kantor-Uriel N, Naaman R, Waldeck DH 2016. The electron's spin and molecular chirality—How are they related and how do they affect life processes?. Chem. Soc. Rev. 45:6478–87
    [Google Scholar]
  130. 130.
    Naaman R, Waldeck DH 2012. Chiral-induced spin selectivity effect. J. Phys. Chem. Lett. 3:2178–87
    [Google Scholar]
  131. 131.
    Zwang TJ, Hurlimann S, Hill MG, Barton JK 2016. Helix-dependent spin filtering through the DNA duplex. J. Am. Chem. Soc. 138:15551–54
    [Google Scholar]
  132. 132.
    Michaeli K, Beratan DN, Waldeck DH, Naaman R 2019. Voltage-induced long-range coherent electron transfer through organic molecules. PNAS 1165931–36
  133. 133.
    Seeman NC 2016. Structural DNA Nanotechnology Cambridge, UK: Cambridge Univ. Press
  134. 134.
    Hong F, Zhang F, Liu Y, Yan H 2017. DNA origami: scaffolds for creating higher order structures. Chem. Rev. 117:12584–640
    [Google Scholar]
  135. 135.
    Wagenbauer KF, Sigl C, Dietz H 2017. Gigadalton-scale shape-programmable DNA assemblies. Nature 552:78–83
    [Google Scholar]
/content/journals/10.1146/annurev-physchem-042018-052353
Loading
/content/journals/10.1146/annurev-physchem-042018-052353
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error