Water-oxidation catalysis by manganese in a geochemical-like cycle

Abstract

Water oxidation in all oxygenic photosynthetic organisms is catalysed by the Mn4CaO4 cluster of Photosystem II. This cluster has inspired the development of synthetic manganese catalysts for solar energy production. A photoelectrochemical device, made by impregnating a synthetic tetranuclear-manganese cluster into a Nafion matrix, has been shown to achieve efficient water oxidation catalysis. We report here in situ X-ray absorption spectroscopy and transmission electron microscopy studies that demonstrate that this cluster dissociates into Mn(II) compounds in the Nafion, which are then reoxidized to form dispersed nanoparticles of a disordered Mn(III/IV)-oxide phase. Cycling between the photoreduced product and this mineral-like solid is responsible for the observed photochemical water-oxidation catalysis. The original manganese cluster serves only as a precursor to the catalytically active material. The behaviour of Mn in Nafion therefore parallels its broader biogeochemistry, which is also dominated by cycles of oxidation into solid Mn(III/IV) oxides followed by photoreduction to Mn2+.

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Figure 1: Comparison of Mn K-edge XAS spectra.
Figure 2: Comparison of electro-oxidized products in Nafion and those of natural and synthetic birnessites.
Figure 3: Comparison of the EXAFS spectra of the electro-oxidized product of [Mn4O4L6]+ in Nafion (black) to a series of standards (grey).
Figure 4: High-resolution transmission electron microscopy images.
Figure 5: Comparison of XANES spectra during various states of catalytic cycling.

References

  1. 1

    Bard, A. J. & Fox, M. A. Artificial photosynthesis: solar splitting of water to hydrogen and oxygen. Acc. Chem. Res. 28, 141–145 (1995).

    CAS  Article  Google Scholar 

  2. 2

    Yano, J. et al. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314, 821–825 (2006).

    CAS  Article  Google Scholar 

  3. 3

    Kok, B., Forbush, B. & McGLoin, M. Cooperation of charges in photosynthetic O2 evolution-I: a linear four step mechanism. Photochem. Photobiol. 11, 457 (1970).

    CAS  Article  Google Scholar 

  4. 4

    Dismukes, G. C. et al. Development of bioinspired Mn4O4-cubane water oxidation catalysts: lessons from photosynthesis. Acc. Chem. Res. 42, 1935–1943 (2009).

    CAS  Article  Google Scholar 

  5. 5

    Tice, M. M. & Lowe, D. R. Photosynthetic microbial matis in the 3,416-Myr-old ocean. Nature 431, 549 (2004).

    CAS  Article  Google Scholar 

  6. 6

    Schopt, J. W. New evidence of the antiquity of life. Origins Life Evol. B. 24, 263–282 (2007).

    Google Scholar 

  7. 7

    Sauer, K. & Yachandra, V. K. A possible evolutionary origin for the Mn4 cluster of the photosynthetic water oxidation complex from natural MnO2 precipitates in the early ocean. Proc. Natl Acad. Sci. 99, 8631–8636 (2002).

    CAS  Article  Google Scholar 

  8. 8

    Hazen, R. M. et al. Mineral evolution. Am. Min. 93, 1693–1720 (2008).

    CAS  Article  Google Scholar 

  9. 9

    Dismukes, G. C. & Blankenship, R. E. The origin and evolution of photosynthetic oxygen production. Adv. Photosynth. Res. 22, 683–695 (2005).

    CAS  Article  Google Scholar 

  10. 10

    Brimblecombe, R., Koo, A., Dismukes, G. C., Swiegers, G. F. & Spiccia, L. Solar-driven water oxidation by a bio-inspired manganese molecular catalyst. J. Am. Chem. Soc. 132, 2892–2894 (2010).

    CAS  Article  Google Scholar 

  11. 11

    Lubitz, W., Reijerse, E. J. & Messinger, J. Solar water-splitting into H2 and O2: design principles of photosystem II and hydrogenases. Energy Envir. Sci. 1, 15–31 (2008).

    CAS  Article  Google Scholar 

  12. 12

    Russel, M. J. & Hall, A. J. Evolution of Early Earth's Atmosphere, Hydrosphere and Biosphere: Constraints from Ore Deposits (eds Kesler, S. E. & Ohmoto, H.) 1–33 (Geological Society of America, 2006).

  13. 13

    Kanan, M. W. & Nocera, D. G. In situ formation of an oxygen-evolving catalyst in neutral water containing phosphate and Co2+. Science 321, 1072–1075 (2008).

    CAS  Article  Google Scholar 

  14. 14

    Yin, Q. et al. A fast soluble carbon-free molecular water oxidation catalyst based on abundant metals. Science 328, 342–345 (2010).

    CAS  Article  Google Scholar 

  15. 15

    Najoafpour, M. M., Ehrenberg, T., Wiechen, M. & Kurz, P. Calcium manganese(III) oxides (CaMn2O4.xH2O) as biomimetic oxygen-evolving catalysts. Angew. Chem. Int. Ed. 49, 2233–2237 (2010).

    Article  Google Scholar 

  16. 16

    Yamazaki, H., Shouji, S., Kajita, A. & Yagi, M. Electrocatalytic and photocatalytic water oxidation to dioxygen based on metal complexes. Coord. Chem. Rev. 254, 2483–2491 (2010).

    CAS  Article  Google Scholar 

  17. 17

    Jiao, F. & Frei, H. Nanostructure manganese oxide clusters supported on mesoporous silica as efficient oxygen-evolving catalysts. Chem. Commun. 46, 2920–2922 (2010).

    CAS  Article  Google Scholar 

  18. 18

    Geletii, Y. V. et al. Homogeneous light-driven water oxidation catalyzed by a tetraruthenium complex with all inorganic ligands. J. Am. Chem. Soc. 131, 7522–7523 (2009).

    CAS  Article  Google Scholar 

  19. 19

    Sartorel, A. et al. Water oxidation at a tetraruthenate core stabilized by polyoxometalate ligands: experimental and computational evidence to trace the competent intermediates. J. Am. Chem. Soc. 131, 16051–16053 (2009).

    CAS  Article  Google Scholar 

  20. 20

    Limburg, J. et al. A functional model for O-O bond formation by the O2-evolving complex in photosystem II. Science 283, 1524–1527 (1999).

    CAS  Article  Google Scholar 

  21. 21

    Concepcion, J. J., Tsai, M.-K., Muckerman, J. T. & Meyer, T. J. Mechanism of water oxidation by single-site ruthenium complex catalysts. J. Am. Chem. Soc. 132, 1545–1557 (2010).

    CAS  Article  Google Scholar 

  22. 22

    Cape, J. L., Lymar, S. V., Lightbody, T. & Hurst, J. K. Characterization of intermediary redox states of the water oxidation catalyst, [Ru(bpy)2(OH2)]2O4+. Inorg. Chem. 48, 4400–4410 (2009).

    CAS  Article  Google Scholar 

  23. 23

    McDaniel, N. D., Coughlin, F. J., Tinker, L. L. & Bernhard, S. Cyclometalated iridium(III) aquo complexes: efficient and tunable catalysts for the homogeneous oxidation of water. J. Am. Chem. Soc. 130, 210–217 (2008).

    CAS  Article  Google Scholar 

  24. 24

    Youngblood, W. J. et al. Photoassisted overall water splitting in a visible light-absorbing dye-sensitized photoelectrochemical cell. J. Am. Chem. Soc. 131, 926–927 (2009).

    CAS  Article  Google Scholar 

  25. 25

    Li, L. et al. A photoelectrochemical device for visible light driven water splitting by a molecular ruthenium catalyst assembled on dye-sensitized nanostructured TiO2 . Chem. Commun. 46, 7307–7309 (2010).

    CAS  Article  Google Scholar 

  26. 26

    Brimblecombe, R., Swiegers, G. F., Dismukes, G. C. & Spiccia, L. Sustained water oxidation photocatalysis by a bioinspired manganese cluster. Angew. Chem. Int. Ed. 47, 7335–7338 (2008).

    CAS  Article  Google Scholar 

  27. 27

    Brimblecombe, R. et al. Sustained water oxidation by [Mn4O4]7+ core complexes inspired by oxygenic photosynthesis. Inorg. Chem. 48, 7269–7279 (2009).

    CAS  Article  Google Scholar 

  28. 28

    Brimblecombe, R., Bond, A. M., Dismukes, G. C., Swiegers, G. F. & Spiccia, L. Electrochemical investigation of Mn4O4-cubane water-oxidizing clusters. Phys. Chem. Chem. Phys. 11, 6441–6449 (2009).

    CAS  Article  Google Scholar 

  29. 29

    Brimblecombe, R., Koo, A., Swiegers, G. F., Dismukes, G. C. & Spiccia, L. ChemSusChem 3, 1146–1150 (2010).

    CAS  Article  Google Scholar 

  30. 30

    Tebo, B. M. et al. Biogenic manganese oxides. Annu. Rev. Earth. Planet. Sci. 32, 287–328 (2004).

    CAS  Article  Google Scholar 

  31. 31

    Saratovsky, I., Wightman, P. G., Pasten, P. A., Gaillard, J-F. & Poeppelmeier, K. R. Manganese oxides: Parallels between abiotic and biotic structures. J. Am. Chem. Soc. 128, 11188–11198 (2006).

    CAS  Article  Google Scholar 

  32. 32

    Webb, S. M., Tebo, B. M. & Bargar, J. R. Structural characterization of biogenic manganese oxides produced in sea water by the marine bacillus sp., strain SG-1. Am. Min. 90, 1342–1357 (2005).

    CAS  Article  Google Scholar 

  33. 33

    Spiro, T. G., Bargar, J. R., Sposito, G. & Tebo, B. M. Bacteriogenic manganese oxides. Acc. Chem. Res. 43, 2–9 (2010).

    CAS  Article  Google Scholar 

  34. 34

    Sunda, W. G. & Huntsman, S. A. Photoreduction of manganese oxides in seawater. Mar. Chem. 46, 133–152 (1994).

    CAS  Article  Google Scholar 

  35. 35

    Sunda, W. G., Huntsman, S. A. & Harvey, G. R. Photoreduction of manganese oxides in seawater and its geochemical and biological implications. Nature 301, 234–236 (1983).

    CAS  Article  Google Scholar 

  36. 36

    Webb, S. M., Tebo, B. M. & Barger, J. R. Structual influence of sodium and calcium ions on biogenic manganese oxides produced by the marine bacillus sp., strain SG-1. Geomicrobiology J. 22, 181–193 (2005).

    CAS  Article  Google Scholar 

  37. 37

    Villalobos, M., Toer, B., Bargar, J. & Sposito, G. Characterization of manganese oxide produce by Psedo-monas putida strain MnB1. Geochim. Cosmochim. Acta 67, 2649–2662 (2003).

    CAS  Article  Google Scholar 

  38. 38

    Kwon, K. D., Refson, K. & Sposito, G. Defect-Induced photoconductivity in layered manganese oxides: a density functional theory study. Phys. Rev. Lett. 100, 146601 (2008).

    Article  Google Scholar 

  39. 39

    Kwon, K. D., Refson, K. & Sposito, G. On the role of Mn(IV) vacancies in the photoreductive dissolution of hexagonal birnesite. Geochim. Cosmochim. Acta 73, 4142–4150 (2009).

    CAS  Article  Google Scholar 

  40. 40

    Gaillot, A-C. et al. Structure of synthetic K-rich birnessite obtained by high-temperature decomposition of KMnO4. I. two-layer polytype from 800 °C experiment. Chem. Mater. 15, 4666–4678 (2003).

    CAS  Article  Google Scholar 

  41. 41

    Masaharu, N., Sayaka, K., Tagashira, H. & Kotaro, O. Electrochemical synthesis of layered manganese oxides intercalated with tetraalkylammonium Ions. Langmuir 21, 354–359 (2005).

    Article  Google Scholar 

  42. 42

    McKeown, D. A. & Post, J. E. Characterization of manganese oxide mineralogy in rock varnish and dendrites using X-ray absorption spectroscopy. Am. Min. 86, 701–713 (2001).

    CAS  Article  Google Scholar 

  43. 43

    Ruettinger, W. F. & Dismukes, G. C. Conversion of core oxos to water molecules by 4e/4H+ reductive dehydration of the Mn4O26+ core in the manganese-oxo cubane complex Mn4O4(Ph2PO2)6: a partial model for photosynthetic water binding and activation. Inorg. Chem. 39, 1021–1027 (2000).

    CAS  Article  Google Scholar 

  44. 44

    Feng, Q. & Waki, H. 31P NMR Study on the binding isomers of chromium(III) phosphinate complexes in solution. Polyhedron 9, 1555–1559 (1990).

    CAS  Article  Google Scholar 

  45. 45

    Lutterman, D. A., Surendranath, Y. & Nocera, D. G. A self-healing oxygen-evolving catalyst. J. Am. Chem. Soc. 131, 3838–3839 (2009).

    CAS  Article  Google Scholar 

  46. 46

    Ruettinger, W., Campana, C. & Dismukes, G. C. Synthesis and characterization of Mn4O4L6 complexes with cubane-like core structure: a new class of models of the active site of the photosynthetic water oxidase. J. Am. Chem. Soc. 119, 6670–6671 (1997).

    CAS  Article  Google Scholar 

  47. 47

    Carrell, T. G., Bourles, E., Lin, M. & Dismukes, G. C. Transition from hydrogen atom to hydride abstraction by Mn4O4(O2PPh2)6 versus [Mn4O4(O2PPh2)6]+: O-H bond dissociation energies and the formation of [Mn4O3(OH)(O2PPh2)6]. Inorg. Chem. 42, 2849–2858 (2003).

    CAS  Article  Google Scholar 

  48. 48

    Cooper, S. R. & Calvin, M. Mixed valence interactions in di-m-oxo bridged manganese complexes. J. Am. Chem. Soc. 99, 6623–6624 (1977).

    CAS  Article  Google Scholar 

  49. 49

    Average (Australian National Beam-line Facility and the Australian Synchrotron, 2008–2010). Available via http://go.nature.com/vZdoeU

  50. 50

    Tenderholt, A., Hedman, B. & Hodgson, K. O. in XAFS13. 105–107 (AIP, 2007).

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Acknowledgements

M. Belousoff and K. Morgan are thanked for their assistance with the collection of the XAS data, D. Desbois and P. Nichols for assistance with the NMR experiments, B. Johannessen, G. Foran, S. P. Best, R. D. Britt, G. C. Dismukes and G. F. Swiegers for helpful discussions, and M. Ma for proof reading the manuscript. We acknowledge the operational support of the High Energy Accelerator Research Organisation (KEK) in Tsukuba, Japan and access to the Australian National Beam-line Facility. We acknowledge financial support from the Australian Research Council through the Australian Centre of Excellence for Electromaterials Science as well as the Linkage Infrastructure, Equipment and Facilities and Discovery Programs (L.S. and R.K.H.), the US DOE (W.H.C.) and US NSF (W.H.C.). B. Birch and the staff at the Melbourne Museum are thanked for the gift of mineral samples M38218 and 6512 from their collection.

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R.K.H. and L.S. proposed the research. R.K.H. participated in the development of the concept of this research, performed the XAS experiments, the NMR experiments, generated samples, analysed the data and co-wrote the manuscript. R.B. participated in the development of the concept of this research, generated samples for analysis and performed some of the XAS experiments. S.L.Y.C. participated in the development of TEM methodology, and performed the TEM experiments. A.S. prepared samples for TEM measurements and measured the photo-current data on catalytic systems. M.H.C and C.G. provided critical advice and assistance with the design of the XAS experiments. W.H.C and L.S. participated in the development of the concept of this research and co-wrote the manuscript.

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Correspondence to Rosalie K. Hocking or Leone Spiccia.

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Hocking, R., Brimblecombe, R., Chang, LY. et al. Water-oxidation catalysis by manganese in a geochemical-like cycle. Nature Chem 3, 461–466 (2011). https://doi.org/10.1038/nchem.1049

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