Electron Tunneling in Biology: When Does it Matter?

Sarhangi, Setare Mostajabi; Matyushov, Dmitry V.

doi:10.20944/preprints202211.0232.v1

Cited by 3 publications

(4 citation statements)

References 82 publications

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“…This view is actually the standard perspective for electron transfer in proteins, but sometimes needs to be corrected for polarizability 96 and/or dynamical effects. 107 All these physical constraints are satisfied by computations published to date (Tables S2, S3, S7). For example, the present author found previously that the electronic couplings, reaction free energies, and reorganization free energies for the Omc-E, S, and Z filaments were respectively <0.015 eV, <|0.28| eV, and 0.48 -0.98 eV.…”

Section: Discussionmentioning

confidence: 75%

“…and GmP reside in the solvent-controlled dynamical regime between a hopping and band-theory description. 107 Mobile electrons appear to propagate through GsW51W57 and GmP too quickly for thermal equilibration of the environment to make the hops independent (memoryless). 122 Because GsP and GsW51W57 are respectively claimed 3,29 now to be the Omc-S and Z filaments for which the structures are known, the following subsections consider (1) If a hopping mechanism applies to electron transfers in OmcS, why have all theoretical works using a hopping mechanism based on the CryoEM structure [71][72][73][74] failed to reproduce the experimentally-derived k %PP ?…”

Section: Unphysically Large Electron Transfer Rates May Be An Experim...mentioning

confidence: 99%

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Are Electrical Characterizations Consistent with the Cytochrome Structures ofGeobacter‘Nanowires’

Guberman-Pfeffer

2023

Preprint

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Electrically conductive filaments from Geobacter sulfurreducens were reported to be pili with metallic-like conductivity, and yet were later shown to be redox-active cytochromes by cryogenic electron microscopy. It has recently been argued that the filaments were simply misidentified, implying that key observations formerly used to refute the involvement of cytochromes in conductivity now must be ascribed to them. Herein, the temperature, pH, voltage, crystallinity, charge propagation, and aromatic density-related dependencies of the conductivity reported for putative pili are re-examined in light of the CryoEM structures of cytochrome filaments. It is demonstrated that: (1) Electrons flow through cytochrome filaments in a succession of redox reactions for which the energetics are physically constrained and the kinetics are largely independent of protein identity for highly conserved heme packing geometries. Computed heme-to-heme electron transfer rates in cytochrome filaments agree, on average, within a factor of 10 of rates experimentally determined in other multi-heme proteins with the same heme packing geometries. (2) T-stacked heme pairs, which comprise nearly or exactly half of all heme pairs in cytochrome filaments are electronic coupling-constrained bottlenecks for electron transfer that set the rate-limiting reaction to the microsecond timescale, which is fast enough compared to typical millisecond enzymatic turnover. Tuning the conductivity of cytochromes over the reported ~10x7-fold range for filaments from G. sulfurreducens strains with pili variants seems both physically implausible and physiologically irrelevant if those filaments are supposed to be cytochromes. (3) The protein-limited flux for redox conduction through a 300-nm filament of T- and slip-stacked heme pairs is predicted to be ~0.1 pA; a G. sulfurreducens cell discharging ~1 pA/s would need at least 10 filaments, which is consistent with experimental estimates of filament abundance. The experimental currents for the Omc- S and Z filaments at a physiologically relevant 0.1 V bias, however, are ~10 pA and ~10 nA, respectively. Some of the discrepancy is attributable to the experimental conditions of a dehydrated protein adsorbed on a bear Au-electrode that contacts ~10x2 hemes, and in the case of conducting probe atomic force microscopy, is crushed under forces known to deform and change the electron transport mechanism through more highly-structured proteins. (4) Previously observed hallmarks of synthetic organic metallic-like conductivity ascribed to pili are inconsistent with the structurally resolved cytochrome filaments under physiological conditions, including (I) increased crystallinity promoting electron delocalization, (II) carbon nanotube-like charge propagation, and (III) an exponential increase-then-decrease in conductivity upon cooling, which was only explain by a model predicted on redox potentials known to be experimentally false. Furthermore, spectroscopic structural characterizations of OmcZ that attest to a huge acid-induced transition to a more crystalline state enhancing conductivity either strongly disagree with CryoEM analyses at higher pH values or give inconclusive results that can be overly interpreted. Overall, a significant discrepancy currently exists - not between theory and experiment - but between the CryoEM cytochrome filament structure in one hand and the other functional characterizations of Geobacter 'nanowires' in the other. The CryoEM structures, theoretical models, biological experiments, and kinetic analyses are all in agreement about the nature and rate of electron transfer in multi-heme architectures under physiological conditions, and stand opposed to the solid-state functional characterizations of Geobacter filaments reported to date. The physiological relevance and/or physical plausibility of some experiments should be examined further.

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Section: Discussionmentioning

confidence: 75%

Section: Unphysically Large Electron Transfer Rates May Be An Experim...mentioning

confidence: 99%

Are Electrical Characterizations Consistent with the Cytochrome Structures ofGeobacter‘Nanowires’

Guberman-Pfeffer

2023

Preprint

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“…In biol-ogy, tunneling effects are observed in protons, electrons, and whole atoms. [99] The two versions of electron tunneling are termed elastic and inelastic; the main difference is that there is no net energy loss in the former, while some energy is lost in the latter. Elastic tunneling (ET) involves tunneling electrons between two metal electrodes separated by a small gap.…”

Section: The Quantum Theory Of Olfactionmentioning

confidence: 99%

The complexities of ligand/receptor interactions: Exploring the role of molecular vibrations and quantum tunnelling

Pagán

2024

BioEssays

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Molecular vibrations and quantum tunneling may link ligand binding to the function of pharmacological receptors. The well‐established lock‐and‐key model explains a ligand's binding and recognition by a receptor; however, a general mechanism by which receptors translate binding into activation, inactivation, or modulation remains elusive. The Vibration Theory of Olfaction was proposed in the 1930s to explain this subset of receptor‐mediated phenomena by correlating odorant molecular vibrations to smell, but a mechanism was lacking. In the 1990s, inelastic electron tunneling was proposed as a plausible mechanism for translating molecular vibration to odorant physiology. More recently, studies of ligands’ vibrational spectra and the use of deuterated ligand analogs have provided helpful information to study this admittedly controversial hypothesis in metabotropic receptors other than olfactory receptors. In the present work, based in part on published experiments from our laboratory using planarians as an experimental organism, I will present a rationale and possible experimental approach for extending this idea to ligand‐gated ion channels.

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“…A definition of tunneling is useful to consider here and it has been described 5 as a "quantum mechanical phenomenon whereby particles can penetrate and pass areas of configuration space with a potential energy higher than their total energy." Operative for electrons 6 as well as hydrogen 7 and even heavier atoms, tunneling explains both unexpected chemistry results and surprisingly accelerated chemical reaction rates, especially at very low temperatures.…”

mentioning

confidence: 99%

Quantum Tunneling in Natural Product Biosynthesis

Filer

2024

Natural Product Communications

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Electron Tunneling in Biology: When Does it Matter?

Cited by 3 publications

References 82 publications

Are Electrical Characterizations Consistent with the Cytochrome Structures ofGeobacter‘Nanowires’

Are Electrical Characterizations Consistent with the Cytochrome Structures ofGeobacter‘Nanowires’

The complexities of ligand/receptor interactions: Exploring the role of molecular vibrations and quantum tunnelling

Quantum Tunneling in Natural Product Biosynthesis

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