Getting to guanine: mechanism and dynamics of charge separation and charge recombination in DNA revisited

Lewis, Frederick D.; Zhu, Huihe; Daublain, Pierre; Sigmund, Karsten; Fiebig, Torsten; Raytchev, Milen; Wang, Qiang; Shafirovich, Vladimir

doi:10.1039/b719715b

Cited by 35 publications

(56 citation statements)

References 40 publications

(36 reference statements)

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“…We also used the coupling and site energy distribution functions described above in the FR model to explore charge transfer in stilbene-capped DNA hairpins studied by Lewis et al (19,41) (Fig. S5).…”

Section: Correlated Vs Uncorrelated Site Energy Fluctuationsmentioning

confidence: 99%

Biological charge transfer via flickering resonance

Zhang¹,

Liu²,

Balaeff³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

153

263

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Biological electron-transfer (ET) reactions are typically described in the framework of coherent two-state electron tunneling or multistep hopping. However, these ET reactions may involve multiple redox cofactors in van der Waals contact with each other and with vibronic broadenings on the same scale as the energy gaps among the species. In this regime, fluctuations of the molecular structures and of the medium can produce transient energy level matching among multiple electronic states. This transient degeneracy, or flickering electronic resonance among states, is found to support coherent (ballistic) charge transfer. Importantly, ET rates arising from a flickering resonance (FR) mechanism will decay exponentially with distance because the probability of energy matching multiple states is multiplicative. The distance dependence of FR transport thus mimics the exponential decay that is usually associated with electron tunneling, although FR transport involves real carrier population on the bridge and is not a tunneling phenomenon. Likely candidates for FR transport are macromolecules with ET groups in van der Waals contact: DNA, bacterial nanowires, multiheme proteins, strongly coupled porphyrin arrays, and proteins with closely packed redox-active residues. The theory developed here is used to analyze DNA charge-transfer kinetics, and we find that charge-transfer distances up to three to four bases may be accounted for with this mechanism. Thus, the observed rapid (exponential) distance dependence of DNA ET rates over distances of K K K K15 Å does not necessarily prove a tunneling mechanism.vibronic coupling | resonant tunneling pathways | superexchange | coherence | gated transport C hemical structure and, importantly, structural fluctuations determine the mechanism and kinetics of charge transfer. Redox energy fluctuations are of particular significance when transport barrier heights and the energy fluctuations are of similar magnitude. Indeed, the sensitivity of biological electrontransfer (ET) rates to conformational fluctuations and consequent (transient) delocalization is the topic of intense interest (1-3). Resonant enhancement of biological ET rates is consistent with a growing body of physical and structural data found in DNA ET through stacked nucleobases (4), extended delocalized structures of bacterial photosynthesis (including the special pair, bridging chlorophyll and pheophytin) (5), the polaronic states of oxidized porphyrin arrays up to seven porphyrin diameters in spatial extent (6), micrometer-scale bacterial nanowires (7, 8), multiheme oxidoreductases (9, 10), amino acid side chains in ribonucleotide reductase (11), engineered protein-based hopping-chains (12), and centimeter-scale charge-transport chains in filamentous bacteria (13). Here, we describe a transient or flickering resonance (FR) mechanism for ET. The FR mechanism arises when thermal fluctuations produce geometries that enable charge delocalization across the entire structure by bringing the donor (D), bridge (B), and acceptor (...

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Section: Correlated Vs Uncorrelated Site Energy Fluctuationsmentioning

confidence: 99%

Biological charge transfer via flickering resonance

Zhang¹,

Liu²,

Balaeff³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

153

263

View full text Add to dashboard Cite

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“…Recent experiments have demonstrated that the rates of CT processes in DNA hairpins depend not only on the distance between the donor and the acceptor sites but on the base pair sequence (32)(33)(34)(35)(36)(37). In particular, it has been found that sequences containing both guanine:cytosine (G:C) and adenine:thymine (A:T) base pairs exhibit a faster hole transfer between S a and S b than sequences involving only A:T base pairs (32,33).…”

mentioning

confidence: 99%

“…In particular, it has been found that sequences containing both guanine:cytosine (G:C) and adenine:thymine (A:T) base pairs exhibit a faster hole transfer between S a and S b than sequences involving only A:T base pairs (32,33). This increase of the arrival rate was attributed to the low ionization potential (IP) of the G base, which is 0.5 eV smaller than the IP reported for adenine molecules (38, 39).…”

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confidence: 99%

Impact of a single base pair substitution on the charge transfer rate along short DNA hairpins

Renaud

Berlin

Ratner

2013

Proc. Natl. Acad. Sci. U.S.A.

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Numerical studies of hole migration along short DNA hairpins were performed with a particular emphasis on the variations of the rate and quantum yield of the charge separation process with the location of a single guanine:cytosine (G:C) base pair. Our calculations show that the hole arrival rate increases as the position of the guanine:cytosine base pair shifts from the beginning to the end of the sequence. Although these results are in agreement with recent experimental findings, the mechanism governing the charge migration along these sequences is revisited here. Instead of the phenomenological two-step hopping mechanism via the guanine base, the charge propagation occurs through a delocalization of the hole density along the base pair stack. Furthermore, the variations of the charge transfer with the position of the guanine base are explained by the impact of the base pair substitutions on the delocalized conduction channels.quantum filling | photoinduced hole transfer | stochastic surrogate Hamiltonian D espite a rather long history, investigations of excess charge carriers in DNA remain an area of intensive experimental and theoretical research (reviewed in refs. 1-3). This interest is mainly due to the relevance of the charge transfer (CT) phenomenon to the oxidation damage (4, 5) and to the potential application of DNA in nanoelectronics (6, 7). Experimentally, charge migration through DNA can be probed either by steady-state methods based on measurements of the damage ratio (8-10) or by time-resolved spectroscopic techniques (11)(12)(13)(14). The latter experimental approach was shown to be particularly efficient for monitoring charge motion in DNA hairpins (13). To carry out time-resolved spectroscopic experiments on these small DNA model systems, the opposite ends of the hairpin are capped with stilbene linkers S a and S b , serving as the hole donor and acceptor, respectively. It has been demonstrated that photoexcitation of S a results in the formation of a bound electron-hole pair initially localized on the hole donor. The separation of this pair occurs via the migration of the hole along the hairpin and the subsequent reaction of the positive charge with the stilbene acceptor. Kinetics of the hole arrival at S b , monitored by a second pulse, enable one to deduce the hole arrival rate, k a , and the quantum yield, Φ a , of the charge separation process.Hole migration along hairpins with less than three base pairs is discussed in terms of a single-step superexchange (15-18). In contrast, multistep sequential hopping is assumed to be responsible for charge propagation along longer hairpins (19-23). The competition between these two mechanisms leads to a distance dependence of the hole arrival rate given by:where N is the number of base pairs in the sequence, κ 1 and κ 2 are scaling factors, R 0 = 3:4 A is the mean interbase pair distance, β = 0:5 − 1:0 A −1 is the exponential falloff parameter for the superexchange mechanism (24-29), and η = 1:5 − 2:0 is the exponent of the power law characteristic f...

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“…The loss of an electron converts DNA to its radical cation (an electron "hole"), which migrates reversibly through duplex DNA by hopping until it is trapped in an irreversible chemical reaction to form a structurally modified base [95]. The dominant mechanism for radical cation migration in DNA is multi-step hopping [113,172] where charge resides on a single base or on small number of adjacent bases and thermal fluctuations precipitate its movement from one base to another [96]. Superexchange is possible, but less effective for long distances, whereby charge is transported coherently in one step by tunnelling [13,157] from a donor to an acceptor through intervening bridging nucleobases [92].…”

Section: Oxidation Of Dnamentioning

confidence: 99%