# Presentation: 587434

## Electron Transfer at the Cytochrome / Mineral Interface:

- Pacific Northwest National Laboratory
- U.S. Department of Energy

**Electron Transfer at the Cytochrome / Mineral Interface:**

**An Overview of the EMSL BGC Modeling Component**

- Rosso K.M., Kerisit S., Valiev M., Wang X., Dupuis M.
*Pacific Northwest National Laboratory*
**ERSD PI Meeting – April 2006**
- Acknowledgements:  US-DOE-OBER-ERSD-EMSL
- EMSL Molecular Sciences Computing Facility
- EMSL NWChem Project

## Current Conceptual Model for Electron Transfer to Extracellular Substrates in Shewanella

***BGC Hypothesis:****  Outer membrane cytochromes OmcA/MtrC are responsible for direct electron transfer to the Fe(III) oxide*

- Courtesy - D. Richardson

**Notes:**
The tetraheme c-type cytochrome, CymA, from Shewanella oneidensis MR-1 has previously
been shown to be required for respiration with Fe(III), nitrate, and fumarate [Myers, C. R., and Myers, J.
M. (1997) J. Bacteriol. 179, 1143-1152]. It is located in the cytoplasmic membrane where the bulk of
the protein is exposed to the periplasm, enabling it to transfer electrons to a series of redox partners. We
have expressed and purified a soluble derivative of CymA (CymAsol) that lacks the N-terminal membrane
anchor. We show here, by direct measurements of electron transfer between the purified proteins, that
CymAsol efficiently reduces S. oneidensis fumarate reductase. This indicates that no further proteins are
required for electron transfer between the quinone pool and fumarate if we assume direct reduction of
CymA by quinols. By expressing CymAsol in a mutant lacking CymA, we have shown that this soluble
form of the protein can complement the defect in fumarate respiration. We also demonstrate that CymA
is essential for growth with DMSO (dimethyl sulfoxide) and for reduction of nitrite, implicating CymA
in at least five different electron transfer pathways in Shewanella.

## Science Questions

*Bis-histidine heme*

*Fe-terminated hematite (001)*

**What regulates the ET rate across the cytochrome/Fe(III)-oxide interface?**
**How are Fe(III) acceptor sites ‘regenerated’ and how fast?**

## Obstacles / Challenges

*Bis-histidine heme*

*Fe-terminated hematite (001)*

- electron transfer distance
- heme electronic structure
- axial ligand orientation
- heme orientation
- porphyrin distortion
- intervening / bridging molecules
- surface atomic structure
- surface electronic structure
- electron transfer distance
- crystallographic direction
-  proximity to surface plane
-  surface termination
-  surface hydration
- defects

**Aspects influencing the ET kinetics at the molecular scale:**

## Basic Electron Transfer Theory

**Basic Electron Transfer Theory**

## Basic Electron Transfer Theory

- ET rate = electronic part + nuclear part

- nuclear

- electronic

- Details of the molecular environment strongly influence the PES’s and electronic coupling

## Electron Migration at Hematite Surfaces

**Electron Migration at Hematite Surfaces**

- Hydroxylated hematite (001)

- Hematite surfaces examined
- Fe-terminated (001)
- O(H)-terminated (001)
- (012)

## Approach to Model the Interatomic Interactions

- The method is based on the **Born model of solids**.

**2****nd**** Term - Short range interactions**
- Electron cloud repulsion,
- Van der Waals, bond stretch,
- angle bend, torsion...

**1****st**** Term - Long range interactions**
- Coulombic energy

**Buckingham Potential:**

**Shell Model****1****:**

- 1Dick and Overhauser *Phys. Rev.*, 112, 90, **1958**.

## Approach to Compute the PES’s:MD + Umbrella Sampling

- ΔE is calculated for each configuration
- As configurations with **Δ****E~0 are rare**, umbrella sampling technique is used to obtained a complete distribution.
- Calculations are carried out for several values of θ (from 0 to 1).

**Approach to Compute the PES’s:****MD + Umbrella Sampling**

- 300 Kelvin
- λTOTAL is obtained directly

- Kerisit and Rosso, JCP, *123*, 224712, **2005**

## Approach for Computing the Electronic Coupling

- Zero Kelvin – without ZPE
- λI and λE obtained separately

- Minimize reactant and product configurations

- E(normal)
- E(reversed)

- E(normal)
- E(reversed)

## {01.2} Hematite Surface - Hydrated

- Water molecules: ~350
- Water slab thickness: ~25 Å

- Lower activation energy at the surface
- Great driving force at the surface
- First interlayer transfer is uphill
- Rapid convergence to bulk value

## Electron Transfer at the{01.2} Hematite Surface

| Direction | ΔG0 (eV) | ΔG* (eV) | VAB (eV) | i | ket (s-1) |
| --- | --- | --- | --- | --- | --- |
| Basal 1 | -1.04 | 0.14 | 0.031 | 2 | 4.9E+11 |
| Basal 2 | 0.20 | 0.55 | 0.184 | 1 | 1.5E+07 |
| Basal (bulk) | 0.00 | 0.46 | 0.184 | 3 | 1.5E+09 |
| C direction | -1.07 | 0.14 | 0.028 | 1 | 2.5E+11 |
| C dir. (bulk) | 0.00 | 0.49 | 0.028 | 1 | 6.6E+07 |

**LAYER 1**

## Summary of Hematite Surface Results

- Water significantly affects the free energy when in direct contact with Fe(III) electron transfer centers and is able to from a short bond with the surface (*e.g*. (012) surface).

- Different surfaces exhibit different behaviors due to different orientations.
- Surface termination affects electron transfer some distance down into the surface.
- Undercoordinated terminal iron atoms can act as electron traps at the surface.

- (001) Hematite Surface

**Summary of Hematite Surface Results**

- Electrons migrate through the surface of hematite no slower than 107 s1.
- The details of the mineral surface structure are critical for controlling the electron migration rate

## Heme / Hematite Electron Transfer

- Cluster model for Bis(histidine) Heme
- FeP(Im)20/+1
- NATOMS= 55

## Heme / Hematite Electron Transfer

- Iron Termination: [Fe11033H33]0/-1

- Hydroxyl Termination: [Fe8030H36]0/-1

**Heme / Hematite Electron Transfer**

- Hematite surface cluster models:

## Heme / Hematite Electron Transfer

**External Part: Continuum Model**
- Marcus’ equation for ET across interfaces*
- EXT. = 0.46-0.71 eV (7-14 Å range)
******TOT.**** = 1.91- 2.16 eV**
- * Marcus JPC (1990)

**Heme / Hematite Electron Transfer**

- Need a simple approach to simulate the repolarization behavior of the surrounding protein and mineral at the interface:

## Heme / Hematite Electron Transfer

**Heme operation potentials of OmcA from *****S. Oneidensis***
- -66 mV, -149 mV, -212 mV in 3:3:4 heme ratio
- (B.J.N. Jepson et al.)
**Flat band potential of hematite anodes in 2 M NaOH solution**
- -426 mV v NHE at pH 13.6
- (Quinn et al. J. Mater. Res. Bull. *11*, 1011-1017, **1976**)
**“****59 mV per unit pH change”**
- (J.K. Leland and A.J. Bard J. Phys. Chem. *91*, 5076-5083, **1987**)
**pH of point of zero charge of hematite** ~ 8
- (L. Cromieres et al. Colloids Surfaces A: Physicochem. Eng. Aspects *202*, 101-115, **2002**)
**Hematite redox potential v NHE at pH****PZC****= -95 mV**

| Free Energy of ET (Heme=>Hematite) |  |
| --- | --- |
| Heme Potential (mV) | G0 (mV) |
| -66 | 29 |
| -149 | -54 |
| -212 | -117 |

**Heme / Hematite Electron Transfer**

## Heme / Hematite Electron Transfer

- NWChem
- Unrestricted Hartree-Fock Level
- Fe Ahlrichs VTZ
- C,O,N,H 6-31G*
- NATOMS= 129 or 132

**Heme / Hematite Electron Transfer**

## Heme / Hematite Electron Transfer

- Hydroxylated hematite (001)

**Heme / Hematite Electron Transfer**

## Heme / Hematite Electron Transfer

**Heme / Hematite Electron Transfer**

## Heme / Hematite Electron Transfer

|  
Distance | Hydroxyl Termination |  |  | Iron Termination |  |  |
| --- | --- | --- | --- | --- | --- | --- |
|  | 1 | 2 | 3 | 1 | 2 | 3 |
| 7 | 1.5E+03 | 1.8E+04 | 1.7E+03 | 4.0E-01 | 1.0E+05 | 2.2E+03 |
| 8 | 9.8E+01 | 3.5E+02 | 3.1E+01 | 8.1E-02 | 7.0E+03 | 2.5E+02 |
| 9 | 1.5E+00 | 1.3E+01 | 7.6E-01 | 5.1E-03 | 4.0E+02 | 4.1E+01 |
| 10 | 1.4E-02 | 3.1E+00 | 3.3E-01 | 5.3E-04 | 2.7E+01 | 2.6E+00 |
| 11 | - | 4.3E-01 | 2.3E-02 | - | 1.7E+00 | 1.3E-01 |

**Rate (s****-1****) for ****Δ****G****0**** = -54 mV**

|  
Distance | Hydroxyl Termination |  |  | Iron Termination |  |  |
| --- | --- | --- | --- | --- | --- | --- |
|  | 1 | 2 | 3 | 1 | 2 | 3 |
| 7 | 1.5E+03 | 1.8E+04 | 1.7E+03 | 4.0E-01 | 1.0E+05 | 2.2E+03 |
| 8 | 9.8E+01 | 3.5E+02 | 3.1E+01 | 8.1E-02 | 7.0E+03 | 2.5E+02 |
| 9 | 1.5E+00 | 1.3E+01 | 7.6E-01 | 5.1E-03 | 4.0E+02 | 4.1E+01 |
| 10 | 1.4E-02 | 3.1E+00 | 3.3E-01 | 5.3E-04 | 2.7E+01 | 2.6E+00 |
| 11 | - | 4.3E-01 | 2.3E-02 | - | 1.7E+00 | 1.3E-01 |

**Heme / Hematite Electron Transfer**

- Hematite (001) surface

## Heme / Hematite Summary

- Electron transfer is fastest when the edge of the porphyrin ring is orientated towards the surface.
- The electron transfer rate decays an order of magnitude with every Å increase in distance.
- Surface termination affects the rate: for most orientations, electron transfer is faster for Fe-termination.

**Heme / Hematite Summary**

- Delivery of electrons to the hematite surface is slower than electron migration through the surface.
- More protein-specific information is needed to select conditions appropriate for comparison with experimental results.

## Current Directions – KMC Models

- 1,000,000 KMC steps - 3D periodic boundary conditions
- Temperature = 300 K
- 4096 iron sites: 1, 2, 4, 8, 16, 32, 64,128 and 256 charge carriers

- 0.03

**Current Directions – KMC Models**

## Current Directions – Heme Environment

** ****NWChem QM/MM module (M. Valiev)**
** ****QM region - 109 atoms (DFT/B3LYP)**
** ****MM region ~ 77000 atoms**
** ****Separate calculation for each of four hemes**
** ****Structural and electronic properties**
** ****Redox potentials**
** ****IR spectra, ....**

**IFC3**

**Current Directions – Heme Environment**

- IFC3  flavin domain  STC