Photosynthesis: from natural to artificial

Ten years ago, the themed issue ‘Biophysical Studies of Photosystem II and Related Model Systems’ was published in PCCP.¹ It was based on an international meeting held in the fall of 2003 in Bad Honnef, Germany, in which, among many other excellent presentations, James Barber presented his 3.5 Å PSII crystal structure for the first time.² Despite its title, the 2004 themed issue almost exclusively covered work done on the natural system, photosystem II. The past decade has seen a tremendous increase in our knowledge about photosystem II and the mechanism by which it oxidizes water to molecular oxygen and hydrogen equivalents. Key to this development was certainly the 1.9 Å resolution crystal structure of photosystem II that was published in 2011,³ since it revealed the water splitting site in atomic detail and thus removed many of the previous uncertainties. This structure formed a firm basis for the elucidation of the water splitting reaction. In parallel, tremendous progress in quantum chemical and spectroscopic methods was achieved. This allowed combining mass spectrometric, spectroscopic and structural results into molecular mechanisms for water oxidation in photosystem II.^4–6 Yet, important questions remain, for example, with regard to structural changes of the Mn₄CaO₅ cluster during the catalytic cycle, the binding sites of the two substrate waters, the nature of the transient states prior to S₄ formation, the structure of the S₄ state and the mode of O–O bond formation, i.e. nucleophilic attack vs. radical coupling. A promising new experimental approach is combined serial femtosecond X-ray crystallography and spectroscopy that is performed with X-ray free electron lasers. The first such studies on photosystem II indicate that it will be possible to obtain radiation damage free structures of all intermediates with this technique.^7,8 Many of the above topics are addressed in the photosystem II related papers in this issue.

The increased knowledge about water oxidation in photosystem II has greatly stimulated the development of artificial catalysts that mimic this process. Prime examples are inorganic Co oxides and CaMn oxides.^9–11 The publications of the Nocera group had a tremendous impact on this field: while they were not the first to show that Co-oxides are good water oxidation catalysts, they presented a simple method for in situ catalyst formation that was put into the context of concepts derived from biological water oxidation.¹² The idea of constructing ‘artificial leaves’ was a great inspiration and guided many of us into the rapidly growing field of artificial photosynthesis. The previous strict divisions between solar cell research, material sciences, (photo)electrochemical cells and photosynthesis are presently breaking down and are replaced by a common and dynamic effort to develop the energy systems of the future, which convert solar light directly into solar fuels such as hydrogen, methane or alcohols like methanol or ethanol. This technique thus promises to address the demand for fuels, which currently cover about 80% of the energy demand. The development from natural to artificial photosynthesis is dramatically reflected in the submissions we received for this themed issue: more than 2/3 of the papers deal with artificial photosynthesis!

Sadly, we also lost in the past 10 years several of our colleagues. Two of them, who contributed to the 2004 themed issue, we would like to honor here: Gernot Renger and Warwick Hillier.

Gernot Renger (23.10.1937–12.01.2013) obtained his doctoral degree in the group of Horst Witt at the TU Berlin, Germany. He thus belonged to the ‘Urgestein’ of biophysical photosynthesis research in general, and of the investigation of photosystem II and photosynthetic water oxidation in particular. Gernot made tremendous contributions to the understanding of the kinetic and thermodynamic aspects of photosynthetic water oxidation, and has written numerous excellent reviews on this.¹³ He had an unsurpassed knowledge of the photosynthesis literature and was always strictly against oversimplifications in the interpretation of data. In many instances, his thinking was well ahead of the mainstream. His friendly and enthusiastic personality has inspired many young scientists in the field of photosynthesis.

Gernot Renger (1937–2013)

Warwick Hillier (18.10.1967–10.01.2014) obtained his PhD in the group of Tom Wydrzynski at the ANU in Canberra, Australia. Subsequently he was a postdoc in the lab of Gerald T. Babcock (Michigan, USA), and then became an associate professor at the ANU. Warwick made seminal contributions to the understanding of substrate water binding to the Mn₄CaO₅ cluster in photosystem II and also developed in Babcock's lab the technique for obtaining FTIR spectra of the different S states of the Kok cycle.^14,15 He had a very broad scientific interest that ranged from evolutionary aspects to astronomy. Warwick loved building novel instrumentation, and more recently also got involved in the utilization of cyanobacteria for bioenergy production. Together with Tom Wydrzynski, he edited in 2012 a book on ‘Molecular Solar Fuels’.¹⁶ His friendly, calm and authentic personality made him a much-admired and highly-praised researcher in the field of photosynthesis. In 2007, he received the Robin Hill award of the International Society for Photosynthesis Research.

Warwick Hillier (1967–2014)

We would like to thank all authors, reviewers and the editorial staff for their contributions to this special issue that documents the forefront of natural and artificial photosynthesis.

References

1. Themed Issue on Biophysical Studies on Photosystem II and Related Model Systems, ed. W. Lubitz and J. Messinger, Phys. Chem. Chem. Phys. , 2004, 6.
2. K. N. Ferreira, T. M. Iverson, K. Maghlaoui, J. Barber and S. Iwata, Science, 2004, 303, 1831–1838.
3. Y. Umena, K. Kawakami, J. R. Shen and N. Kamiya, Nature, 2011, 473, 55–61.
4. N. Cox, D. A. Pantazis, F. Neese and W. Lubitz, Acc. Chem. Res., 2013, 46, 1588–1596.
5. N. Cox and J. Messinger, Biochim. Biophys. Acta, Bioenerg., 2013, 1827, 1020–1030.
6. P. E. M. Siegbahn, Acc. Chem. Res., 2009, 42, 1871–1880.
7. J. Kern, R. Alonso-Mori, R. Tran, J. Hattne, R. J. Gildea, N. Echols, C. Glöckner, J. Hellmich, H. Laksmono, R. G. Sierra, B. Lassalle-Kaiser, S. Koroidov, A. Lampe, G. Y. Han, S. Gul, D. DiFiore, D. Milathianaki, A. R. Fry, A. Miahnahri, D. W. Schafer, M. Messerschmidt, M. M. Seibert, J. E. Koglin, D. Sokaras, T. C. Weng, J. Sellberg, M. J. Latimer, R. W. Grosse-Kunstleve, P. H. Zwart, W. E. White, P. Glatzel, P. D. Adams, M. J. Bogan, G. J. Williams, S. Boutet, J. Messinger, A. Zouni, N. K. Sauter, V. K. Yachandra, U. Bergmann and J. Yano, Science, 2013, 340, 491–495.
8. J. Kern, R. Alonso-Mori, J. Hellmich, R. Tran, J. Hattne, H. Laksmono, C. Glöckner, N. Echols, R. G. Sierra, J. Sellberg, B. Lassalle-Kaiser, R. J. Gildea, P. Glatzel, R. W. Grosse-Kunstleve, M. J. Latimer, T. A. McQueen, D. DiFiore, A. R. Fry, M. Messerschmidt, A. Miahnahri, D. W. Schafer, M. M. Seibert, D. Sokaras, T. C. Weng, P. H. Zwart, W. E. White, P. D. Adams, M. J. Bogan, S. Boutet, G. J. Williams, J. Messinger, N. K. Sauter, A. Zouni, U. Bergmann, J. Yano and V. K. Yachandra, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 9721–9726.
9. M. W. Kanan and D. G. Nocera, Science, 2008, 321, 1072–1075.
10. M. M. Najafpour, T. Ehrenberg, M. Wiechen and P. Kurz, Angew. Chem., Int. Ed., 2010, 49, 2233–2237.
11. D. M. Robinson, Y. B. Go, M. Mui, G. Gardner, Z. J. Zhang, D. Mastrogiovanni, E. Garfunkel, J. Li, M. Greenblatt and G. C. Dismukes, J. Am. Chem. Soc., 2013, 135, 3494–3501.
12. D. G. Nocera, Acc. Chem. Res., 2012, 45, 767–776.
13. G. Renger, Biochim. Biophys. Acta, Bioenerg., 2012, 1817, 1164–1176.
14. W. Hillier and T. Wydrzynski, Coord. Chem. Rev., 2008, 252, 306–317.
15. W. Hillier and G. T. Babcock, Biochemistry, 2001, 40, 1503–1509.
16. Molecular Solar Fuels, ed. T. J. Wydrzynski and W. Hillier, The Royal Society of Chemistry, Cambridge, 2012.

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