Biological charge transfer via flickering resonance

Abstract

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 (...

Engineering nanometre-scale coherence in soft matter

“…28)). However, incoherent CT rates scale with V 2 (as expected from Fermi's golden rule 6,29 ), so the resistance that arises in an incoherent mechanism is expected to be more sensitive to changes in V. This line of analysis motivated the sequence design ds-5ʹC n G n 3ʹ ds-5ʹG n C n 3ʹ ds-5ʹC n G n 3ʹ Figure 3 | Cross-strand G-G overlaps and computed resistance for ds-5′C n G n 3′ and ds-5′G n C n 3′. a, Sequence of ds-5′C n G n 3′ (n = 3) and cross-stranded guanine structure in the conformation G\G.…”

“…The ds-5′C n G n 3′ (n = 3-8) resistance oscillations are consistent with a phenomenological transport model that invokes partial charge-transfer (CT) coherence 10 . The recent experimental findings for the ds-5′C n G n 3′ (n = 3-8) chains are not consistent with most conventional models for DNA charge transport, as most models predict incoherent hopping over distances of about six base pairs or more 11 , although some recent studies indicate a possible role for partial or transient delocalization 6,12 .…”

“…Indeed, the considerable excitement that surrounds quantum effects in photobiology [2][3][4] and in DNA charge transport 5 is because they derive fundamentally from spatially extended coherence. Coherence and delocalization can be persistent or fleeting 6 , depending on the scale of the interactions and the disorder in the local environments.…”

Using coherence to enhance function in chemical and biophysical systems

“…Coherence and decoherence are, therefore, competing processes; see Box 1. To understand conceptually how energy gap fluctuations affect resonances and, upon appropriate averaging, give rise to decoherence, the example of "flickering resonance" can be helpful 19 . Adding wave amplitudes, or interference phenomena, has dramatic consequences.…”

Could tyrosine and tryptophan serve multiple roles in biological redox processes?

“…We suggest that appropriately placed tyrosine (Tyr) and/or tryptophan (Trp) residues can prevent such damage by rapid reduction of the intermediates followed by transfer of the oxidizing equivalent to less harmful sites or out of the protein altogether [28]. A protective role of this sort will not Work by theorists has shed much light on the main factors controlling biological ET reactions [34,35]: and, in our experimental programme, we have found semiclassical ET theory [36] to be particularly useful in analyses of results. Notably, given a particular spatial arrangement of redox cofactors, we can predict driving force dependences of the relative time constants for single-step (τ ss = 1/k ss ) and multi-step (τ hop ) electron transport [31].…”