The Role of Microorganisms in Iron Reduction in Marine Sediments

2023

J. Phys. Chem. B

Structural determinants of a 103-fold variation in electrical conductivity for helical homopolymers of tetra-, hexa-, and octa-heme cytochromes (named Omc- E, S, and Z, respectively) from Geobacter sulfurreducens are investigated with the Pathways model for electron tunneling, classical molecular dynamics, and hybrid quantum/classical molecular mechanics. Thermally averaged electronic couplings for through-space heme-to-heme electron transfer in the “nanowires” computed with density functional theory are ≤0.015 eV. Pathways analyses also indicate that couplings match within a factor of 5 for all “nanowires”, but some alternative tunneling routes are found involving covalent protein backbone bonds (Omc- S and Z) or propionic acid-ligating His H-bonds on adjacent hemes (OmcZ). Reorganization energies computed from electrostatic vertical energy gaps or a version of the Marcus continuum expression parameterized on the total (donor + acceptor) solvent-accessible surface area typically agree within 20% and fall within the range 0.48–0.98 eV. Reaction free energies in all three “nanowires” are ≤|0.28| eV, even though Coulombic interactions primarily tune the site redox energies by 0.7–1.2 eV. Given the conserved energetic parameters, redox conductivity differs by < 103-fold among the cytochrome “nanowires”. Redox currents do not exceed 3.0 × 10–3 pA at a physiologically relevant 0.1 V bias, with the slowest electron transfers being on a (μs) timescale much faster than typical (ms) enzymatic turnovers. Thus, the “nanowires” are proposed to be functionally robust to variations in structure that provide a habitat-customized protein interface. The 30 pA to 30 nA variation in conductivity previously reported from atomic force microscopy experiments is not intrinsic to the structures and/or does not result from the physiologically relevant redox conduction mechanism.

Section: Introductionmentioning

confidence: 99%

Structural Determinants of Redox Conduction Favor Robustness over Tunability in Microbial Cytochrome Nanowires

2023

J. Phys. Chem. B

“…The nearest electron donor/acceptor in some aquatic sediments, however, is either another microbe or a mineral nanoparticle that may be up to a few microns away. Coupling the reduction of microbes or minerals in the extracellular space with intracellular oxidative metabolism constitutes an ancient and widespread respiratory strategy. − The electrical circuits established between microbes and minerals, if better understood, can elucidate the biogeochemical evolution of the planet, − the role of the microbiome in human health and diseases, − as well as templates − for the design of bioelectronic technologies. − …”

Section: Introductionmentioning

confidence: 99%

Assessing Thermal Response of Redox Conduction for Anti-Arrhenius Kinetics in a Microbial Cytochrome Nanowire

2022

J. Phys. Chem. B

A micrometers-long helical homopolymer of the outer-membrane cytochrome type S (OmcS) from Geobacter sulfurreducens is proposed to transport electrons to extracellular acceptors in an ancient respiratory strategy of biogeochemical and technological significance. OmcS surprisingly exhibits higher conductivity upon cooling (anti-Arrhenius kinetics), an effect previously attributed to H-bond restructuring and heme redox potential shifts. Herein, the temperature sensitivity of redox conductivity is more thoroughly examined with conventional and constant-redox and -pH molecular dynamics and quantum mechanics/ molecular mechanics. A 30 K drop in temperature constituted a weak perturbation to electron transfer energetics, changing electronic couplings (⟨H mn ⟩), reaction free energies (ΔG mn ), reorganization energies (λ mn ), and activation energies (E a ) by at most |0.002|, |0.050|, |0.120|, and |0.045| eV, respectively. Changes in ΔG mn reflected −0.07 ± 0.03 V shifts in redox potentials that were caused in roughly equal measure by altered electrostatic interactions with the solvent and protein.Changes in intraprotein H-bonding reproduced the earlier observations. Single-particle diffusion and multiparticle steady-state flux models, parametrized with Marcus theory rates, showed that biologically relevant incoherent hopping cannot qualitatively or quantitatively describe electrical conductivity measured by atomic force microscopy in filamentous OmcS. The discrepancy is attributed to differences between solution-phase simulations and solid-state measurements and the need to model intra-and intermolecular vibrations explicitly.

“…Cytochrome ‘nanowires’ are polymeric multi-heme cytochromes that catalyze the transfer of electrons across microbe-microbe 1 and microbe-mineral 2–5 interfaces. As terminal reductases in a widespread respiratory strategy 6,7 of biogeochemical significance, 2–5 and promising materials for bioelectronic technologies, 8–15 cytochrome ‘nanowires’ have attracted much recent interest.…”

mentioning

confidence: 99%

Structural Determinants of Redox Conduction Favor Robustness over Tunability in Microbial Cytochrome Nanowires

2023

Preprint

Helical homopolymers of multiheme cytochromes catalyze biogeochemically significant electron transfers with a reported 10 to the 3-fold variation in conductivity. Herein, classical molecular dynamics and hybrid quantum/classical molecular mechanics are used to elucidate the structural determinants of the redox potentials and conductivities of the tetra-, hexa-, and octaheme outer-membrane cytochromes E, S, and Z, respectively, from Geobacter sulfurreducens. Second-sphere electrostatic interactions acting on minimally polarized heme centers are found to regulate redox potentials over a computed 0.5-V range. However, the energetics of redox conduction are largely robust to structural diversity: Single-step electronic couplings ([less than H greater than), reaction free energies (DeltaG), and reorganization energies (lambda) are always respectively less than |0.026|, less than |0.26|, and between 0.5 - 1.0 eV. With these conserved parameter ranges, redox conductivity differed by less than a factor of 10 among the nanowires and is sufficient to meet the demands of cellular respiration if 10 to the 2 to 10 to the 3 nanowires are expressed. The nanowires are proposed to be differentiated by the protein packaging to interface with a great variety of environments, and not by conductivity, because the rate-limiting electron transfers are elsewhere in the respiratory process. Conducting-probe atomic force microscopy measurements that find conductivities 10 to the 3-10 to the 6-fold more than cellular demands are suggested to report on functionality that is either not used or not accessible under physiological conditions. The experimentally measured difference in conductivity between Omc- S and Z is suggested to not be an intrinsic feature of the CryoEM-resolved structures.