skip to main content

Title: Intrinsic electronic conductivity of individual atomically resolved amyloid crystals reveals micrometer-long hole hopping via tyrosines

Proteins are commonly known to transfer electrons over distances limited to a few nanometers. However, many biological processes require electron transport over far longer distances. For example, soil and sediment bacteria transport electrons, over hundreds of micrometers to even centimeters, via putative filamentous proteins rich in aromatic residues. However, measurements of true protein conductivity have been hampered by artifacts due to large contact resistances between proteins and electrodes. Using individual amyloid protein crystals with atomic-resolution structures as a model system, we perform contact-free measurements of intrinsic electronic conductivity using a four-electrode approach. We find hole transport through micrometer-long stacked tyrosines at physiologically relevant potentials. Notably, the transport rate through tyrosines (105s−1) is comparable to cytochromes. Our studies therefore show that amyloid proteins can efficiently transport charges, under ordinary thermal conditions, without any need for redox-active metal cofactors, large driving force, or photosensitizers to generate a high oxidation state for charge injection. By measuring conductivity as a function of molecular length, voltage, and temperature, while eliminating the dominant contribution of contact resistances, we show that a multistep hopping mechanism (composed of multiple tunneling steps), not single-step tunneling, explains the measured conductivity. Combined experimental and computational studies reveal that proton-coupled electron transfer more » confers conductivity; both the energetics of the proton acceptor, a neighboring glutamine, and its proximity to tyrosine influence the hole transport rate through a proton rocking mechanism. Surprisingly, conductivity increases 200-fold upon cooling due to higher availability of the proton acceptor by increased hydrogen bonding.

« less
; ; ; ; ; ; ; ; ; ;
Award ID(s):
Publication Date:
Journal Name:
Proceedings of the National Academy of Sciences
Page Range or eLocation-ID:
Article No. e2014139118
Proceedings of the National Academy of Sciences
Sponsoring Org:
National Science Foundation
More Like this
  1. Resonant tunneling diodes (RTDs) have come full-circle in the past 10 years after their demonstration in the early 1990s as the fastest room-temperature semiconductor oscillator, displaying experimental results up to 712 GHz and fmax values exceeding 1.0 THz [1]. Now the RTD is once again the preeminent electronic oscillator above 1.0 THz and is being implemented as a coherent source [2] and a self-oscillating mixer [3], amongst other applications. This paper concerns RTD electroluminescence – an effect that has been studied very little in the past 30+ years of RTD development, and not at room temperature. We present experiments and modeling of an n-type In0.53Ga0.47As/AlAs double-barrier RTD operating as a cross-gap light emitter at ~300K. The MBE-growth stack is shown in Fig. 1(a). A 15-μm-diam-mesa device was defined by standard planar processing including a top annular ohmic contact with a 5-μm-diam pinhole in the center to couple out enough of the internal emission for accurate free-space power measurements [4]. The emission spectra have the behavior displayed in Fig. 1(b), parameterized by bias voltage (VB). The long wavelength emission edge is at  = 1684 nm - close to the In0.53Ga0.47As bandgap energy of Ug ≈ 0.75 eV at 300 K.more »The spectral peaks for VB = 2.8 and 3.0 V both occur around  = 1550 nm (h = 0.75 eV), so blue-shifted relative to the peak of the “ideal”, bulk InGaAs emission spectrum shown in Fig. 1(b) [5]. These results are consistent with the model displayed in Fig. 1(c), whereby the broad emission peak is attributed to the radiative recombination between electrons accumulated on the emitter side, and holes generated on the emitter side by interband tunneling with current density Jinter. The blue-shifted main peak is attributed to the quantum-size effect on the emitter side, which creates a radiative recombination rate RN,2 comparable to the band-edge cross-gap rate RN,1. Further support for this model is provided by the shorter wavelength and weaker emission peak shown in Fig. 1(b) around = 1148 nm. Our quantum mechanical calculations attribute this to radiative recombination RR,3 in the RTD quantum well between the electron ground-state level E1,e, and the hole level E1,h. To further test the model and estimate quantum efficiencies, we conducted optical power measurements using a large-area Ge photodiode located ≈3 mm away from the RTD pinhole, and having spectral response between 800 and 1800 nm with a peak responsivity of ≈0.85 A/W at  =1550 nm. Simultaneous I-V and L-V plots were obtained and are plotted in Fig. 2(a) with positive bias on the top contact (emitter on the bottom). The I-V curve displays a pronounced NDR region having a current peak-to-valley current ratio of 10.7 (typical for In0.53Ga0.47As RTDs). The external quantum efficiency (EQE) was calculated from EQE = e∙IP/(∙IE∙h) where IP is the photodiode dc current and IE the RTD current. The plot of EQE is shown in Fig. 2(b) where we see a very rapid rise with VB, but a maximum value (at VB= 3.0 V) of only ≈2×10-5. To extract the internal quantum efficiency (IQE), we use the expression EQE= c ∙i ∙r ≡ c∙IQE where ci, and r are the optical-coupling, electrical-injection, and radiative recombination efficiencies, respectively [6]. Our separate optical calculations yield c≈3.4×10-4 (limited primarily by the small pinhole) from which we obtain the curve of IQE plotted in Fig. 2(b) (right-hand scale). The maximum value of IQE (again at VB = 3.0 V) is 6.0%. From the implicit definition of IQE in terms of i and r given above, and the fact that the recombination efficiency in In0.53Ga0.47As is likely limited by Auger scattering, this result for IQE suggests that i might be significantly high. To estimate i, we have used the experimental total current of Fig. 2(a), the Kane two-band model of interband tunneling [7] computed in conjunction with a solution to Poisson’s equation across the entire structure, and a rate-equation model of Auger recombination on the emitter side [6] assuming a free-electron density of 2×1018 cm3. We focus on the high-bias regime above VB = 2.5 V of Fig. 2(a) where most of the interband tunneling should occur in the depletion region on the collector side [Jinter,2 in Fig. 1(c)]. And because of the high-quality of the InGaAs/AlAs heterostructure (very few traps or deep levels), most of the holes should reach the emitter side by some combination of drift, diffusion, and tunneling through the valence-band double barriers (Type-I offset) between InGaAs and AlAs. The computed interband current density Jinter is shown in Fig. 3(a) along with the total current density Jtot. At the maximum Jinter (at VB=3.0 V) of 7.4×102 A/cm2, we get i = Jinter/Jtot = 0.18, which is surprisingly high considering there is no p-type doping in the device. When combined with the Auger-limited r of 0.41 and c ≈ 3.4×10-4, we find a model value of IQE = 7.4% in good agreement with experiment. This leads to the model values for EQE plotted in Fig. 2(b) - also in good agreement with experiment. Finally, we address the high Jinter and consider a possible universal nature of the light-emission mechanism. Fig. 3(b) shows the tunneling probability T according to the Kane two-band model in the three materials, In0.53Ga0.47As, GaAs, and GaN, following our observation of a similar electroluminescence mechanism in GaN/AlN RTDs (due to strong polarization field of wurtzite structures) [8]. The expression is Tinter = (2/9)∙exp[(-2 ∙Ug 2 ∙me)/(2h∙P∙E)], where Ug is the bandgap energy, P is the valence-to-conduction-band momentum matrix element, and E is the electric field. Values for the highest calculated internal E fields for the InGaAs and GaN are also shown, indicating that Tinter in those structures approaches values of ~10-5. As shown, a GaAs RTD would require an internal field of ~6×105 V/cm, which is rarely realized in standard GaAs RTDs, perhaps explaining why there have been few if any reports of room-temperature electroluminescence in the GaAs devices. [1] E.R. Brown,et al., Appl. Phys. Lett., vol. 58, 2291, 1991. [5] S. Sze, Physics of Semiconductor Devices, 2nd Ed. 12.2.1 (Wiley, 1981). [2] M. Feiginov et al., Appl. Phys. Lett., 99, 233506, 2011. [6] L. Coldren, Diode Lasers and Photonic Integrated Circuits, (Wiley, 1995). [3] Y. Nishida et al., Nature Sci. Reports, 9, 18125, 2019. [7] E.O. Kane, J. of Appl. Phy 32, 83 (1961). [4] P. Fakhimi, et al., 2019 DRC Conference Digest. [8] T. Growden, et al., Nature Light: Science & Applications 7, 17150 (2018). [5] S. Sze, Physics of Semiconductor Devices, 2nd Ed. 12.2.1 (Wiley, 1981). [6] L. Coldren, Diode Lasers and Photonic Integrated Circuits, (Wiley, 1995). [7] E.O. Kane, J. of Appl. Phy 32, 83 (1961). [8] T. Growden, et al., Nature Light: Science & Applications 7, 17150 (2018).« less
  2. Conducting probe atomic force microscopy (CP-AFM) was employed to examine electron tunneling in self-assembled monolayer (SAM) junctions. A 2.3 nm long perylene tetracarboxylic acid diimide (PDI) acceptor molecule equipped with isocyanide linker groups was synthesized, adsorbed onto Ag, Au and Pt substrates, and the current–voltage ( I – V ) properties were measured by CP-AFM. The dependence of the low-bias resistance ( R ) on contact work function indicates that transport is LUMO-assisted (‘n-type behavior’). A single-level tunneling model combined with transition voltage spectroscopy (TVS) was employed to analyze the experimental I – V curves and to extract the effective LUMO position ε l = E LUMO − E F and the effective electronic coupling ( Γ ) between the PDI redox core and the contacts. This analysis revealed a strong Fermi level ( E F ) pinning effect in all the junctions, likely due to interface dipoles that significantly increased with increasing contact work function, as revealed by scanning Kelvin probe microscopy (SKPM). Furthermore, the temperature ( T ) dependence of R was found to be substantial. For Pt/Pt junctions, R varied more than two orders of magnitude in the range 248 K < T < 338 K. Importantly,more »the R ( T ) data are consistent with a single step electron tunneling mechanism and allow independent determination of ε l , giving values compatible with estimates of ε l based on analysis of the full I – V data. Theoretical analysis revealed a general criterion to unambiguously rule out a two-step transport mechanism: namely, if measured resistance data exhibit a pronounced Arrhenius-type temperature dependence, a two-step electron transfer scenario should be excluded in cases where the activation energy depends on contact metallurgy. Overall, our results indicate (1) the generality of the Fermi level pinning phenomenon in molecular junctions, (2) the utility of employing the single level tunneling model for determining essential electronic structure parameters ( ε l and Γ ), and (3) the importance of changing the nature of the contacts to verify transport mechanisms.« less
  3. A new electrically conducting 3D metal-organic framework (MOF) with a unique architecture was synthesized using 1,2,4,5-tetrakis-(4-carboxyphenyl)benzene (TCPB) a redox-active cis -dipyridyl-tetrathiafulvalene ( Z -DPTTF) ligand. While TCPB formed Zn 2 (COO) 4 secondary building units (SBUs), instead of connecting the Zn 2 -paddlewheel SBUs located in different planes and forming a traditional pillared paddlewheel MOF, the U-shaped Z -DPTTF ligands bridged the neighboring SBUs formed by the same TCPB ligand like a sine-curve along the b axis that created a new sine -MOF architecture. The pristine sine -MOF displayed an intrinsic electrical conductivity of 1 × 10 −8  S/m, which surged to 5 × 10 −7  S/m after I 2 doping due to partial oxidation of electron rich Z -DPTTF ligands that raised the charge-carrier concentration inside the framework. However, the conductivities of the pristine and I 2 -treated sine -MOFs were modest possibly because of large spatial distances between the ligands that prevented π-donor/acceptor charge-transfer interactions needed for effective through-space charge movement in 3D MOFs that lack through coordination-bond charge transport pathways.
  4. Achieving a molecular-level understanding of how the structures and compositions of metal–organic frameworks (MOFs) influence their charge carrier concentration and charge transport mechanism—the two key parameters of electrical conductivity—is essential for the successful development of electrically conducting MOFs, which have recently emerged as one of the most coveted functional materials due to their diverse potential applications in advanced electronics and energy technologies. Herein, we have constructed four new alkali metal (Na, K, Rb, and Cs) frameworks based on an electron-rich tetrathiafulvalene tetracarboxylate (TTFTC) ligand, which formed continuous π-stacks, albeit with different π–π-stacking and S⋯S distances ( d π–π and d S⋯S ). These MOFs also contained different amounts of aerobically oxidized TTFTC˙ + radical cations that were quantified by electron spin resonance (ESR) spectroscopy. Density functional theory calculations and diffuse reflectance spectroscopy demonstrated that depending on the π–π-interaction and TTFTC˙ + population, these MOFs enjoyed varying degrees of TTFTC/TTFTC˙ + intervalence charge transfer (IVCT) interactions, which commensurately affected their electronic and optical band gaps and electrical conductivity. Having the shortest d π–π (3.39 Å) and the largest initial TTFTC˙ + population (∼23%), the oxidized Na-MOF 1-ox displayed the narrowest band gap (1.33 eV) and the highest room temperature electrical conductivitymore »(3.6 × 10 −5 S cm −1 ), whereas owing to its longest d π–π (3.68 Å) and a negligible TTFTC˙ + population, neutral Cs-MOF 4 exhibited the widest band gap (2.15 eV) and the lowest electrical conductivity (1.8 × 10 −7 S cm −1 ). The freshly prepared but not optimally oxidized K-MOF 2 and Rb-MOF 3 initially displayed intermediate band gaps and conductivity, however, upon prolonged aerobic oxidation, which raised the TTFTC˙ + population to saturation levels (∼25 and 10%, respectively), the resulting 2-ox and 3-ox displayed much narrower band gaps (∼1.35 eV) and higher electrical conductivity (6.6 × 10 −5 and 4.7 × 10 −5 S cm −1 , respectively). The computational studies indicated that charge movement in these MOFs occurred predominantly through the π-stacked ligands, while the experimental results displayed the combined effects of π–π-interactions, TTFTC˙ + population, and TTFTC/TTFTC˙ + IVCT interaction on their electronic and optical properties, demonstrating that IVCT interactions between the mixed-valent ligands could be exploited as an effective design strategy to develop electrically conducting MOFs.« less
  5. Newman, Dianne K. (Ed.)
    ABSTRACT Sideroxydans species are important chemolithoautotrophic Fe(II)-oxidizing bacteria in freshwater environments and play a role in biogeochemical cycling of multiple elements. Due to difficulties in laboratory cultivation and genetic intractability, the electron transport proteins required for the growth and survival of this organism remain understudied. In Sideroxydans lithotrophicus ES-1, it is proposed that the Mto pathway transfers electrons from extracellular Fe(II) oxidation across the periplasm to an inner membrane NapC/NirT family protein encoded by Slit_2495 to reduce the quinone pool. Based on sequence similarity, Slit_2495 has been putatively called CymA, a NapC/NirT family protein which in Shewanella oneidensis MR-1 oxidizes the quinol pool during anaerobic respiration of a wide range of substrates. However, our phylogenetic analysis using the alignment of different NapC/NirT family proteins shows that Slit_2495 clusters closer to NirT sequences than to CymA. We propose the name ImoA (inner membrane oxidoreductase) for Slit_2495. Our data demonstrate that ImoA can oxidize quinol pools in the inner membrane and is able to functionally replace CymA in S. oneidensis. The ability of ImoA to oxidize quinol in vivo as opposed to its proposed function of reducing quinone raises questions about the directionality and/or reversibility of electron flow through the Mto pathwaymore »in S. lithotrophicus. IMPORTANCE Fe(II)-oxidizing bacteria play an important role in biogeochemical cycles. At circumneutral pH, these organisms perform extracellular electron transfer, taking up electrons from Fe(II) outside the cell, potentially through a porin-cytochrome complex in the outer membrane encoded by the Mto pathway. Electrons from Fe(II) oxidation would then be transported to the quinone pool in the inner membrane via periplasmic and inner membrane electron transfer proteins. Directly demonstrating the functionality of genes in neutrophilic iron oxidizers is challenging due to the absence of robust genetic methods. Here, we heterologously expressed a NapC/NirT family tetraheme cytochrome ImoA, encoded by Slit_2495, an inner membrane protein from the Gram-negative Fe(II)-oxidizing bacterium Sideroxydans lithotrophicus ES-1, proposed to be involved in extracellular electron transfer to reduce the quinone pool. ImoA functionally replaced the inner membrane c-type cytochrome CymA in the Fe(III)-reducing bacterium Shewanella oneidensis. We suggest that ImoA may function primarily to oxidize quinol inS. lithotrophicus.« less