Multiheme Cytochrome Mediated Redox Conduction through

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Multiheme Cytochrome Mediated Redox Conduction Through Shewanella oneidensis MR-1 Cells Shuai Xu, Alexandre Barrozo, Leonard M. Tender, Anna I. Krylov, and Mohamed Y. El-Naggar J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.8b05104 • Publication Date (Web): 30 Jul 2018 Downloaded from http://pubs.acs.org on July 30, 2018

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Journal of the American Chemical Society

Multiheme Cytochrome Mediated Redox Conduction Through Shewanella oneidensis MR-1 Cells Shuai Xu,† Alexandre Barrozo,‡ Leonard M. Tender∥, Anna I. Krylov,‡ and Mohamed Y. El-Naggar*†‡§ † Department of Physics and Astronomy, University of Southern California, Los Angeles, California 90089, United States ‡ Department of Chemistry, University of Southern California, Los Angeles, California 90089, United States ∥ Center for Bio/Molecular Science and Engineering, Naval Research Laboratory, Washington, D.C. 20375, United States § Department of Biological Sciences, University of Southern California, Los Angeles, California 91030, United States

ABSTRACT: Multiheme cytochromes function as extra-

cellular electron transfer (EET) conduits that extend the metabolic reach of microorganisms to external solid surfaces. These conduits are also proposed to facilitate longdistance electron transport along cellular membranes and across multiple cells. Here we report electrochemical gating measurements of Shewanella oneidensis MR-1 cells linking interdigitated electrodes. The dependence of the source-drain current on gate potential demonstrates a redox conduction mechanism, which we link to the presence of multiheme cytochromes of the Mtr pathway. We also find that the measured thermal activation energy of 0.29 ± 0.03 eV is consistent with these obtained from electron hopping calculations through the S. oneidensis Mtr outer-membrane decaheme cytochromes. Our measurements and calculations have implications for understanding and controlling micrometer-scale electron transport in microbial systems.

Microorganisms have evolved extracellular electron tranfer (EET) mechanisms to and from surfaces, allowing them to use redox-active minerals outside the cells as electron acceptors or donors for metabolism, or to interact with other cells through interspecies electron transfer.1 In addition to their important environmental role in elemental cycling on a global scale, such microbes are being incorporated into electrodes as living catalysts for renewable energy technologies.2 Both native and engineered EET pathways allow microbes to drive fuel-to-electricity conversion on anodes and reduce CO2 to fuels or other high value products on cathodes powered by renewable electricity.3-4 In order to fully harness this biotechnological potential of microbe-electrode interactions, it is important to understand the underlying molecular pathways such as bacterial multiheme cytochromes that can allow EET across

the biotic-abiotic interface.5 For example, the metal-reducing bacterium Shewanella oneidensis MR-1 relies on the multiheme MtrABC complex as the primary electronconducting conduit across the cell envelope.6 At the cell surface, MtrC and a partnering decaheme cytochrome, OmcA, can act as terminal reductases for external electron-accepting surfaces7 or intermediary soluble redox shuttles8. In addition to allowing cellular respiration at electrode interfaces, EET components may also facilitate long-distance electron transport across neighboring cells.9 This proposal has been supported by conductivity measurements of Geobacter sulfurreducens biofilms, which can exceed tens of microns in thickness.10-14 The electrochemical signature of this conduction, and its temperature dependence, pointed to a mechanism of sequential electron transfer reactions through redox cofactors generally consistent with the hemes of cytochromes.11-12, 15 However, it was not possible to implicate specific cytochromes, given that Geobacter possesses multiple parallel pathways across the cell envelope and through the biofilm,1, 16 including more than 50 multiheme cytochromes and additional EET components such as conductive pili.10, 15-18 These factors complicate the assignment of biofilm conduction to a specific molecular pathway. Here we demonstrate cytochrome-specific micrometerscale electron conduction through S. oneidensis cellular monolayers. S. oneidensis requires the Mtr pathway’s cytochromes for EET to electrodes,8, 19-20 and the now available crystal structures of the outer-membrane decaheme cytochromes (MtrF, MtrC, and OmcA)21-23 have recently enabled calculations of the thermodynamics and kinetics of electron transport along their heme chains.24-26 These molecular-level calculations now allow us to interpret measurements of cytochrome-mediated long-distance electron transport. Specifically, we report electrochemical measurements of conduction through S. oneidensis cells

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bridging electrodes. The conduction peaks at a gate potential corresponding to the formal potential of Mtr proteins, in support of a cytochrome-mediated multistep redox conduction mechanism similar to redox polymers. In addition, we find that this electron transport process is thermally activated, with an activation energy that is consistent with transport through MtrC and MtrF.

Figure 1. Experimental setup. (A) S. oneidensis cells bridge interdigitated source and drain electrodes, with potentials ES and ED. Source current, drain current, and the source-todrain conduction current are measured, in the presence of a small driving voltage (VSD=ED-ES), as a function of gate potential (EG=(ES+ED)/2). (B) Fluorescence image of cells (stained red with FM4-64FX membrane stain) on indium tin oxides (ITO) electrodes. Scale bar: 10 µm.

We cultivated S. oneidensis cells anaerobically in a defined medium as described previously,20 before transfer to a bioelectrochemical reactor that contained an interdigitated microelectrode array (IDA) of indium tin oxide (ITO) source/drain electrode bands patterned on glass and separated by 5 µm gaps (Figure 1A). Both electrodes were first shorted and poised as a single anode (0.44 V vs SHE) for 16 hours to promote cellular attachment.20 Fluorescent and atomic force microscopy revealed that cells

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accumulated on the IDA enough to span the source-drain gap in multiple locations (Figure 1B). Following this electrochemical cultivation period, we probed EET and source-drain conduction using voltammetry and electrochemical gating.11 With both electrode bands still swept as a single anode, turnover cyclic voltammetry (i.e. in the presence of lactate) revealed two catalytic waves as expected for S. oneidensis20; the wave with an onset at -0.23 V corresponds to a flavin dependent mechanism, while that with 0.17 V onset is associated with EET via multiheme cytochromes (Figure S1). After medium exchange with a fresh defined medium, containing lactate but no electron acceptor, turnover voltammetry retained only the higher potential cytochrome-facilitated wave (Figure S1), as expected due to removal of the cellsecreted flavins. Next, we performed electrochemical gating measurements to assess conduction through cells bridging the source and drain electrodes. Here, the source and drain potentials (ES and ED) are controlled by a bipotentiostat and scanned simultaneously at the same rate n, while maintaining a constant small source-drain voltage (VSD = ED-ES). Figure 2A features the measured currents at the source and drain electrodes, using VSD = 0.02 V and n = 1 mV s-1, under both turnover and non-turnover conditions (no electron donor). Under non-turnover conditions, current at each electrode is determined by the VSD-driven source-drain conduction current (Icond) as well as a background contribution from Faradaic charging/discharging of cellular redox cofactors, but without turnover current from catalytic oxidation of lactate. The background contribution is eliminated by one of two methods: (i) subtracting raw source current from raw drain current to yield 2Icond, which assumes the background current is the same for both electrodes in the limit of small VSD, or (ii) performing separate VSD = 0 scans to measure the Faradaic current and subsequently subtracting it from the current observed in the VSD = 0.02 V scan at each electrode (see SI for details).11-12 We cross-checked both methods to show that they yield consistent results (Figure S2), indicating that the observed current peak reflects Icond and not Faradaic current. The gating procedure can be carried out at different temperatures (Figure 2B) to reveal the dependence of cellular conduction on temperature. In Figure 3A, we show the dependence of Icond on gate potential, EG = (ES+ED)/2, in the 4-38 °C range. The observation of a conduction peak at the expected formal potential of the cytochromes (E0’ = 0.18 V vs SHE) is consistent with a redox conduction mechanism where sequential electron transfer steps are driven by a redox gradient across the source-drain gap.11-12, 15 In contrast to this conduction through the 5 um IDA gap, no peak was observed in a control experiment

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using two large split electrodes separated by a 1 mm gap too large to be bridged by cells (Figure S2).

Figure 2. Electrochemical gating measurements (A) Source and drain currents under turnover (lactate present) and nonturnover (no electron donor) conditions as a function of source and drain potentials, respectively. Measurements conditions: source-drain voltage VSD = 0.02 V and scan rate n = 1 mV s-1. (B) Non-turnover measurements at 295.15 K and 311.15 K.

To confirm the assignment of the conduction peak location to the formal potential of cytochromes, we performed voltammetry on an S. oneidensis mutant (DMtr/DmtrB/DmtrE) lacking eight functional periplasmic and outer-membrane cytochromes,27 including the entire Mtr-Omc pathway. As expected, the mutant did not exhibit the clear cytochrome oxidation or reduction peaks obvious in the wild-type (Figure S3). In addition, we tested any possible contribution of soluble components to conduction, by measuring the source-drain current of cellfree spent media obtained after cellular conduction measurements. Soluble factors, including these in the defined medium or cell-secreted redox active components (e.g.

released cytochromes or Fe28), made a negligible contribution to the conduction current compared to cell-covered IDA (Figure S4). These experiments point to conduction primarily mediated by cell-associated multiheme cytochromes.

Figure 3. Conduction measurements. (A) Dependence of conduction current Icond on gate potential EG for different temperatures (Forward gating scans only shown for clarity. Corresponding backward scans shown in Figure S5). (B) Representative Arrehnius-style plot (using peak Icond at EG = E0’) yields an activation energy Ea = 0.29±0.03 eV.

In Figure 3B, we show the dependence of Icond (at EG = E0’) on temperature. By fitting to the expected dependence for an idealized redox conductor at small VSD (Equation 1, where A is a temperature-independent factor),11 we extract the thermal activation energy Ea = 0.29±0.03 (n = 3 separate biological replicates). ,

01

𝐼#$%& = 𝑉*+ - 𝑒 / 23

(1)

This measured activation energy is consistent with values for single-step electron transfer in redox proteins, including cytochromes, especially when cofactors are partially solvent exposed,5 but are higher than previously reported for transport in Geobacter biofilms.11 Next, we



compare our results to specific temperature-dependent stochastic calculations of electron hopping through the decaheme cytochromes MtrC and MtrF. These are the systems for which the thermodynamic parameters and electronic couplings that dictate individual electron transfer steps along their heme chains have been calculated.2426 The ‘staggered-cross’ structure of the Mtr proteins potentially allows four terminal hemes (2, 5, 7 and 10) to serve as ingress/egress sites (Figure S6).21, 23 While EET across the cellular membrane is thought to proceed between hemes 5 and 10 as terminals, the more buried hemes 2 and 7 may allow for interactions with soluble shuttles or additional cofactors such as flavins.21, 23, 29 Recent footprinting measurements also support a role for heme 7 as a donor to external minerals.30 To address multiple possibilities, we used a Kinetic Monte Carlo (KMC) model31 to assess multiple routes by simulating bidirectional electron hopping with various ingress/egress sites: 10↔5, 2↔7, and 10↔7. For the 10↔5 route, we considered two distinct conductance regimes, corresponding to two sets of step-wise electron transfer rates computed for different oxidation states of MtrC/F (see SI for KMC details).26 The first ‘one-electron’ set was derived from calculations with a single heme reduced at a time. The second ‘two-electron’ set was derived similarly but with heme 7, which has the highest redox potential of the 10 hemes, always reduced.26 Table 1. Activation energies (Ea) obtained from KMC simulations of MtrC/F for various heme ingress/egress routes. ‘One-electron’ represents simulations using rates of transfer from the single electron hopping case. ‘Two-electron’ corresponds to a similar scenario, but with heme 7 always reduced. Equation 1 was used for fitting Ea. All values in eV. Flow Route

Ea, MtrC

Ea, MtrF

10→5 (one-electron)

0.299 ± 0.005

0.278 ± 0.005

5→10 (one-electron)

0.315 ± 0.007

0.231 ± 0.003

10→5 (two-electron)

0.309 ± 0.010

0.262 ± 0.003

5→10 (two-electron)

0.31 ± 0.018

0.278 ± 0.010

2→7

0.261 ± 0.016

0.268 ± 0.006

7→2

0.219 ± 0.007

0.272 ± 0.006

10→7

0.237 ± 0.007

0.202 ± 0.003

7→10

0.289 ± 0.010

0.279 ± 0.014

The simulations were performed for 11 temperatures, between 286.15 and 306.15 K. Table 1 shows the overall thermal activation barriers for electron transport, with the majority of routes yielding activation barriers consistent with that measured through cells. Of the routes simulated in MtrC, the dominant terminal reductase for EET, the higher activation barriers of the 10↔5 route make it rate-

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limiting and are in very close agreement with the measured activation energy for cellular conduction (0.29±0.03 eV). Recent observations of the distribution of Shewanella’s periplasmic and outer-membrane cytochromes suggest a collision-exchange model,32 where long-distance transport is facilitated by a combination of electron hopping and intermediate diffusive steps (e.g. lateral cytochrome mobility) to link neighboring cytochromes. While not considering this full complexity, nor accounting for OmcA and periplasmic components, our calculations suggest that the temperature dependence of electron transport through electrode-spanning cells could well be dictated by hopping along cytochrome heme chains rather than intermediate inter-protein events. To summarize, we have found that Shewanella oneidensis MR-1 cells can act as redox conduction channels across electrodes and identified multiheme cytochromes of the Mtr pathway as critical electron conduits that facilitate this conduction. These findings represent a step towards understanding and harnessing biological electron transport over cellular length scales. ASSOCIATED CONTENT Supporting Information. The Supporting Information is available free of charge on the ACS Publications website. Experimental details, computational methodology, additional characterization, and controls (PDF).

AUTHOR INFORMATION Corresponding Author

* [email protected] Notes

The authors declare no competing financial interests.

ACKNOWLEDGMENT S.X. and M.Y.E.-N. acknowledge support by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the US Department of Energy through grant DE-FG02-13ER16415. Microfabrication and imaging are supported by the Air Force Office of Scientific Research grant FA955014-1-0294. A.I.K. acknowledges support by the U.S. National Science Foundation (No. CHE1566428). LMT acknowledges the Office of Naval research for funding (N0001418WX00436). We acknowledge the Extreme Science and Engineering Discovery Environment33 (XSEDE TG-CHE170005) for computational resources at the San Diego Supercomputer Center, and the USC HighPerformance Computing Center.

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25. Breuer, M.; Rosso, K. M.; Blumberger, J., Electron flow in multiheme bacterial cytochromes is a balancing act between heme electronic interaction and redox potentials. P Natl Acad Sci USA 2014, 111 (2), 611-616. 26. Barrozo, A.; El‐Naggar Mohamed, Y.; Krylov Anna, I., Distinct Electron Conductance Regimes in Bacterial Decaheme Cytochromes. Angewandte Chemie International Edition 2018, 57 (23), 6805-6809 27. Coursolle, D.; Gralnick, J. A., Reconstruction of extracellular respiratory pathways for iron(III) reduction in Shewanella oneidensis strain MR-1. Front Microbiol 2012, 3. 28. Oram, J.; Jeuken Lars, J. C., A Re‐evaluation of Electron ‐ Transfer Mechanisms in Microbial Electrochemistry: Shewanella Releases Iron that Mediates Extracellular Electron Transfer. ChemElectroChem 2016, 3 (5), 829-835. 29. Watanabe, H. C.; Yamashita, Y.; Ishikita, H., Electron transfer pathways in a multiheme cytochrome MtrF. Proceedings of the National Academy of Sciences 2017, 114 (11), 2916. 30. Fukushima, T.; Gupta, S.; Rad, B.; Cornejo, J. A.; Petzold, C. J.; Chan, L. J. G.; Mizrahi, R. A.; Ralston, C. Y.; Ajo-Franklin, C. M., The Molecular Basis for Binding of an Electron Transfer Protein to a Metal Oxide Surface. J Am Chem Soc 2017, 139 (36), 12647-12654. 31. Byun, H. S.; Pirbadian, S.; Nakano, A.; Shi, L.; ElNaggar, M. Y., Kinetic Monte Carlo Simulations and Molecular Conductance Measurements of the Bacterial Decaheme Cytochrome MtrF. Chemelectrochem 2014, 1 (11), 1932-1939. 32. Subramanian, P.; Pirbadian, S.; El-Naggar, M. Y.; Jensen, G. J., Ultrastructure of Shewanella oneidensis MR-1 nanowires revealed by electron cryotomography. P Natl Acad Sci USA 2018, 115 (14), E3246-E3255. 33. Towns, J.; Cockerill, T.; Dahan, M.; Foster, I.; Gaither, K.; Grimshaw, A.; Hazlewood, V.; Lathrop, S.; Lifka, D.; Peterson, G. D.; Roskies, R.; Scott, J. R.; WilkinsDiehr, N., XSEDE: Accelerating Scientific Discovery. Computing in Science & Engineering 2014, 16 (5), 62-74.


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Multiheme Cytochrome Mediated Redox Conduction through

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