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+.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Bard, A. J. & Fox, M. A. Artificial photosynthesis: solar splitting of water to hydrogen and oxygen. Acc. Chem. Res. 28, 141–145 (1995).
Yano, J. et al. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314, 821–825 (2006).
Kok, B., Forbush, B. & McGLoin, M. Cooperation of charges in photosynthetic O2 evolution-I: a linear four step mechanism. Photochem. Photobiol. 11, 457 (1970).
Dismukes, G. C. et al. Development of bioinspired Mn4O4-cubane water oxidation catalysts: lessons from photosynthesis. Acc. Chem. Res. 42, 1935–1943 (2009).
Tice, M. M. & Lowe, D. R. Photosynthetic microbial matis in the 3,416-Myr-old ocean. Nature 431, 549 (2004).
Schopt, J. W. New evidence of the antiquity of life. Origins Life Evol. B. 24, 263–282 (2007).
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).
Hazen, R. M. et al. Mineral evolution. Am. Min. 93, 1693–1720 (2008).
Dismukes, G. C. & Blankenship, R. E. The origin and evolution of photosynthetic oxygen production. Adv. Photosynth. Res. 22, 683–695 (2005).
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).
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).
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).
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).
Yin, Q. et al. A fast soluble carbon-free molecular water oxidation catalyst based on abundant metals. Science 328, 342–345 (2010).
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).
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).
Jiao, F. & Frei, H. Nanostructure manganese oxide clusters supported on mesoporous silica as efficient oxygen-evolving catalysts. Chem. Commun. 46, 2920–2922 (2010).
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).
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).
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).
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).
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).
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).
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).
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).
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).
Brimblecombe, R. et al. Sustained water oxidation by [Mn4O4]7+ core complexes inspired by oxygenic photosynthesis. Inorg. Chem. 48, 7269–7279 (2009).
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).
Brimblecombe, R., Koo, A., Swiegers, G. F., Dismukes, G. C. & Spiccia, L. ChemSusChem 3, 1146–1150 (2010).
Tebo, B. M. et al. Biogenic manganese oxides. Annu. Rev. Earth. Planet. Sci. 32, 287–328 (2004).
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).
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).
Spiro, T. G., Bargar, J. R., Sposito, G. & Tebo, B. M. Bacteriogenic manganese oxides. Acc. Chem. Res. 43, 2–9 (2010).
Sunda, W. G. & Huntsman, S. A. Photoreduction of manganese oxides in seawater. Mar. Chem. 46, 133–152 (1994).
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).
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).
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).
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).
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).
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).
Masaharu, N., Sayaka, K., Tagashira, H. & Kotaro, O. Electrochemical synthesis of layered manganese oxides intercalated with tetraalkylammonium Ions. Langmuir 21, 354–359 (2005).
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).
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).
Feng, Q. & Waki, H. 31P NMR Study on the binding isomers of chromium(III) phosphinate complexes in solution. Polyhedron 9, 1555–1559 (1990).
Lutterman, D. A., Surendranath, Y. & Nocera, D. G. A self-healing oxygen-evolving catalyst. J. Am. Chem. Soc. 131, 3838–3839 (2009).
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).
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).
Cooper, S. R. & Calvin, M. Mixed valence interactions in di-m-oxo bridged manganese complexes. J. Am. Chem. Soc. 99, 6623–6624 (1977).
Average (Australian National Beam-line Facility and the Australian Synchrotron, 2008–2010). Available via http://go.nature.com/vZdoeU
Tenderholt, A., Hedman, B. & Hodgson, K. O. in XAFS13. 105–107 (AIP, 2007).
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nchem.1049
This article is cited by
-
Electrocatalytic water oxidation with manganese phosphates
Nature Communications (2024)
-
Self-healing oxygen evolution catalysts
Nature Communications (2022)
-
Investigation of electrocatalytic activity of a new mononuclear Mn(II) complex for water oxidation in alkaline media
Photosynthesis Research (2022)
-
Ultra-small and highly dispersive iron oxide hydroxide as an efficient catalyst for oxidation reactions: a Swiss-army-knife catalyst
Scientific Reports (2021)
-
Efficient degradation of orange II by ZnMn2O4 in a novel photo-chemical catalysis system
Frontiers of Chemical Science and Engineering (2020)