Structural Analysis of the Oxygen Evolving Complex Using Low Frequency SERS Andrew J. Wilson and Prashant K. Jain Department of Chemistry University of Illinois at Urbana-Champaign 21 June 2017 International Symposium on Molecular Spectroscopy Clusters/Complexes Urbana-Champaign, IL

Photosystem II (PSII) Yano et al., Chem. Rev., 2001, 114, 4175-4205 Umena et al., Nature, 2011, 473, 55-60 Govindjee et al., eLS, 2001 PSII is a protein complex which initiates solar-to-chemical energy conversion in photosynthesis The oxygen evolving complex (OEC) splits water with a small overpotential and produces little reactive intermediates

Oxygen Evolving Complex (OEC) Redox Intermediates S0 S1 S2 S3 S4 e- H+ O2 H2O Net reaction: 2H2O  4H+ + 4e- + O2 Umena et al., Nature, 2011, 473, 55-60 What is the protonation of the OEC in S1? What are the intermediate Si structures in operando? Kok et al., Photochem. Photobio., 1970, 11, 457-475

Surface-enhanced Raman scattering (SERS) microscopy Pushing resolution in catalysis S0 S1 S2 S3 S4 Current challenges X-ray beam damage / H-insensitivity Crystals (time/space average, T, physiology) Impure S-state preparation Spatial averaging over samples Surface-enhanced Raman scattering (SERS) microscopy Reduce spatial averaging (~ 0.5 μm) Observe bond breaking/formation in operando Track OEC water ligands air H2O 10 μm

Photosystem II cluster PSII SERS measurement Photosystem II cluster Ag nanoparticle monolayer glass 10 μm 100X 514.5 nm cw laser excitation beam splitter 0.2-1 s / frame Long pass filter spectrometer

Dynamic PSII SERS spectra air air H2O H2O Low Frequency Dynamics

PSII SERS in Water Isotopologues 672 cm-1 664 cm-1 N = 2250 N = 2250 S1 dark-stable state Protonation W2: H2O or OH? O5: O or OH? Use DFT to calculate Raman frequencies using 16OH2/18OH2 ligands Umena et al., Nature, 2011, 473, 55-60

S1 Protonation State: Raman from DFT Model W2: OH O5: O W2: H2O O5: O W2: OH O5: OH W2: H2O O5: OH 16OH2 18OH2 Exp.

S1 Model and SERS SERS 16OH2 18OH2 O5=O, W2= H2O model reproduces 16OH2/18OH2 shift for 672 cm-1: (β HO(W1)-Mn4) DFT Raman spectrum predicts several modes observed in SERS snapshots Observe OEC sample the S1 state Use the protonation of S1 to generate models of S0-S3

S0 Model SERS, S0 Raman (DFT) S0 - H+, - e- S1 S0 Interatomic distances: Pal et al., Biochemistry, 2013, 52, 7703-7706

S2 Model Open Isomer Closed Isomer S1 - e- Interatomic distances: Pantazis et al., Angew. Chem. Int. Ed. 2012, 51, 9935-9940

S3 Model LH Wx Isomer RH Wx Isomer S2 -H+, -e- +H2O Interatomic distances: Askerka et al., Biochemistry, 2016, 55, 981-984

Proposed Intermediates H+ H+ H2O Summary Stay tuned! S4 In operando OEC dynamics S1 protonation using DFT/SERS S0-S3 models S1 e- H+ e- S3 H2O S2 “RH Wx” “open” e- H+

Acknowledgements ▪ Prof. Prashant K. Jain ▪ Dinumol Devasia Funding ▪ Arnold and Mabel O. Beckman Foundation ▪ Springborn Postdoctoral Fellowship