The Biomimetic Inspiration for Renewable Hydrogen Fuel Production from Water Oxidation within Artificial Photosynthesis

Ron J. Pace; Rob Stranger

doi:10.1071/CH11476

RESEARCH FRONT (Open Access)

Previous Next Contents Vol 65(6)

The Biomimetic Inspiration for Renewable Hydrogen Fuel Production from Water Oxidation within Artificial Photosynthesis

Ron J. Pace ^A ^B and Rob Stranger ^A

+ Author Affiliations

- Author Affiliations

^A Research School of Chemistry, College of Physical and Mathematical Sciences, Australian National University, Canberra, ACT 0200, Australia.

^B Corresponding author. Email: Ron.Pace@anu.edu.au

Australian Journal of Chemistry 65(6) 597-607 https://doi.org/10.1071/CH11476
Submitted: 13 December 2011 Accepted: 3 February 2012 Published: 13 April 2012

Abstract

The thermodynamic constraints for the operation of the water oxidizing Mn₄/Ca cluster within Photosystem II (PS II) are discussed. These are then examined in the light of the known redox chemistry of hydrated Mn-oxo systems and relevant model compounds. It is shown that the latest high resolution crystal structure of cyanobacterial PS II suggests an organization of the mono Ca tetranuclear Mn cluster that naturally accommodates the stringent requirements for successive redox potential constancy, with increasing total oxidation state, which the enzyme function imposes. This involves one region of the Mn₄/Ca cluster being dominantly involved with substrate water binding, while a separate, single Mn is principally responsible for the redox accumulation function. Recent high level computational chemical investigations by the authors’ strongly support this, with a computed pattern of Mn oxidation states throughout the catalytic cycle being completely consistent with this interpretation. Strategies to design synthetic, biomimetic constructs utilizing this approach for efficient electrolytic generation of hydrogen fuel within artificial photosynthesis are briefly discussed.

References

[1] R. E. Blankenship, H. Hartman, Trends Biochem. Sci. 1998, 23, 94.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVOms74%3D&md5=fe6fc94aefa1b453e1d38d12b3767ee4CAS |

[2] R. J. Pace, An Integrated Artificial Photosynthesis Model, in Artificial Photosynthesis 2005, Chap. 2 (Eds A. Collings, C. Critchley) (Wiley-VCH: Weinheim).

[3] A. Melis, Plant Sci. 2009, 177, 272.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1KgsrY%3D&md5=1e6610bab2a1457a8cfafa0d36e4ef8dCAS |

[4] K. Satoh, T. Wydrzynski, Govindjee, Photosystem II: The Light Driven Water: Plastoquinone Oxidoreductase 2005 (Springer: Dordrecht, The Netherlands).

[5] (a) (a) C. W. Hoganson, G. T. Babcock, Biological Processes, in Metal Ions in Biological Systems 1999, Volume 37, pp. 613–656 (Eds A. Sigel, H. Sigel) (Marcel Dekker: New York, NY).
(b) (b) D. A. Cherepanov, W. Drevenstedt, L. L. Krishtalik, A. Y. Mulkidjanian, W. Junge, in Photosynthesis: Mechanisms and Effects 1998, Volume II, pp. 1073–1076 (Ed. G. Garab) (Kluwer Academic Publishers: Dortrecht).

[6] W. Hillier, T. Wydrzynski, BBA-Bioenergetics 2001, 1503, 197.
| 1:CAS:528:DC%2BD3cXoslGjtb8%3D&md5=b6e7cef4fc14272af755ab99d0626d84CAS |

[7] M. Haumann, C. Müller, P. Liebisch, L. Iuzzolino, J. Dittmer, M. Grabolle, T. Neisius, W. Meyer-Klaucke, H. Dau, Biochemistry 2005, 44, 1894.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmsVSksw%3D%3D&md5=838aa62173233b6ea9ac1f83035f2818CAS |

[8] F. Rappaport, J. Lavergne, Biochim. Biophys. Acta 2001, 1503, 246.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXoslGjtbo%3D&md5=8f4db7bbe82bde9d4406f8c08bde902eCAS |

[9] Y. Umena, K. Kawakami, J.-R. Shen, N. Kamiya, Nature 2011, 473, 55.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkslCmtLg%3D&md5=f7b48594fae4a870a2b3d1c7ed10df43CAS |

[10] (a) A. Guskov, J. Kern, A. Gabdulkhakov, M. Broser, A. Zouni, W. Saenger, Nat. Struct. Mol. Biol. 2009, 16, 334.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvFKjt7s%3D&md5=13b621fba48ee1ce230fbd2edab6997bCAS |
      (b) B. Loll, J. Kern, W. Saenger, A. Zouni, J. Biesiadka, Nature 2005, 438, 1040.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) K. N. Ferreira, T. M. Iverson, K. Maghlaoui, J. Barber, S. Iwata, Science 2004, 303, 1831.
         | Crossref | GoogleScholarGoogle Scholar |
      (d) N. Kamiya, J. R. Shen, Proc. Natl. Acad. Sci. USA 2003, 100, 98.
         | Crossref | GoogleScholarGoogle Scholar |

[11] S. Luber, I. Rivalta, Y. Umena, K. Kawakami, J.-R. Shen, N. Kamiya, G. W. Brudvig, V. S. Batista, Biochemistry 2011, 50, 6308.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotVars7w%3D&md5=c265cdfd2761756bbb76a822fdda14f5CAS |

[12] P. Gatt, R. Stranger, R. J. Pace, J. Photochem. Photobiol. B 2011, 104, 80.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFWjtrg%3D&md5=ea42e23037a40d151517cd37512dfc19CAS |

[14] P. E. M. Siegbahn, Acc. Chem. Res. 2009, 42, 1871.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlWmu7fJ&md5=0b1085c3dd673167528a43972b7804a2CAS |

[15] E. M. Sproviero, J. A. Gascón, J. P. McEvoy, G. W. Brudvig, V. S. Batista, J. Am. Chem. Soc. 2008, 130, 3428.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlCntL4%3D&md5=b4eda1587d6804886f333e1272a5b367CAS |

[16] V. K. Yachandra, K. Sauer, M. P. Klein, Chem. Rev. 1996, 96, 2927.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xmt1GlsL4%3D&md5=d03e8b8135d0835eebacf3f18c2f96bfCAS |

[17] (a) A. R. Jaszewski, R. Stranger, R. J. Pace, Phys. Chem. Chem. Phys. 2009, 11, 5634.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotFWmsbc%3D&md5=1a930df933e5cf2ce9e99de37a2c2586CAS |
      (b) A. R. Jaszewski, R. Stranger, R. J. Pace, Chem.–Eur. J. 2011, 17, 5699.
         | Crossref | GoogleScholarGoogle Scholar |

[18] K. Yamaguchi, D. T. Sawyer, Inorg. Chem. 1985, 24, 971.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFSjt7g%3D&md5=48e6508d1b98040a545ab8923e298dd6CAS |

[19] S. Mukhopadhyay, S. K. Mandal, S. Bhaduri, W. H. Armstrong, Chem. Rev. 2004, 104, 3981.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnt12iur8%3D&md5=1a57249cc115931d6d3aeb8380925843CAS |

[20] E. Jacobsen, Acc. Chem. Res. 2000, 33, 421.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtFKhsLY%3D&md5=fb1833b0b2b90b6126cc62e4fcc113dfCAS |

[21] (a) M. Kanan, D. Nocera, Science 2008, 321, 1072.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSitrbP&md5=4d554995a8442318e37fd3fd4f64344fCAS |
      (b) Q. Yin, J. M. Tan, C. Besson, Y. V. Geletti, D. Musaev, A. E. Kuznetsov, Z. Luo, K. I. Hardcastle, C. L. Hill, Science 2010, 328, 342.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) F. Jiao, H. Frei, Angew. Chem. Int. Ed. 2009, 48, 1841.
         | Crossref | GoogleScholarGoogle Scholar |
      (d) D. M. Robinson, Y. B. Go, M. Greenblatt, G. C. Dismukes, J. Am. Chem. Soc. 2010, 132, 11467.
         | Crossref | GoogleScholarGoogle Scholar |
      (e) R. K. Hocking, R. Brimblecombe, L.-Y. Chang, A. Singh, M. H. Cheah, C. Glover, W. H. Casey, L. Spiccia, Nat. Chem. 2011, 3, 461.

[22] G. F. Swiegers, J. K. Clegg, R. Stranger, Chem. Sci. 2011, 2, 2254.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12isrvL&md5=2bb497c792c79a23dde60032a1b3c096CAS |

[23] G. L. Elizarova, G. M. Zhidomirov, V. N. Parmon, Catal. Today 2000, 58, 71.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFyqt7k%3D&md5=5740faa55435e1b99b1ef741b07d70c3CAS |

[25] (a) M. W. Kanan, J. Yano, Y. Surendranath, M. Dincă, V. K. Yachandra, D. G. Nocera, J. Am. Chem. Soc. 2010, 132, 13692.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFGru7zM&md5=540cc424d400d53fa31ddfbaffecfcd3CAS |
      (b) M. Risch, V. Khare, I. Zaharieva, L. Gerencser, P. Chernev, H. Dau, J. Am. Chem. Soc. 2009, 131, 6936.
         | Crossref | GoogleScholarGoogle Scholar |

[26] (a) J. W. Murray, J. Barber, J. Struct. Biol. 2007, 159, 228.
         | Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1ygsrk%3D&md5=f9983b6703c87c7e46345cf254c4d179CAS |
      (b) H. Ishikita, W. Saenger, B. Loll, J. Biesiadka, E.-W. Knapp, Biochemistry 2006, 45, 2063.
         | Crossref | GoogleScholarGoogle Scholar |
      (c) F. M. Ho, S. Styring, Biochim. Biophys. Acta 2008, 1777, 140.

[27] A. R. Jaszewski, R. Stranger, R. J. Pace, J. Phys. Chem. B 2011, 115, 4484.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVanu7g%3D&md5=fb61035972be193f134d93450ea6f7b3CAS |

[28] M. R. Razeghifard, R. J. Pace, Biochemistry 1999, 38, 1252.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXos12j&md5=7ebee8b998d8ec53e7b1364c891a5a7aCAS |

[29] J. Buchta, M. Grabolle, H. Dau, BBA-Bioenergetics 2007, 1767, 565.
| 1:CAS:528:DC%2BD2sXmt1ygtrY%3D&md5=33e704dc1b1ff60d130d32433c4762ddCAS |

[30] F. Rappaport, M. Blanchard-Desce, J. Lavergne, BBA-Bioenergetics 1994, 1184, 178.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitFars78%3D&md5=902ac1e361aa55d891f82d5395e366e7CAS |

[32] D. Shevela, K. Beckmann, J. Clausen, W. Junge, J. Messinger, Proc. Natl. Acad. Sci. USA 2011, 108, 3602.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXivFKltL4%3D&md5=f96fad109a7f81c7d001a3e1b27091edCAS |

[33] C. W. Hoganson, N. Lydakis-Simantiris, X.-S. Tang, C. Tommos, K. Warncke, G. T. Babcock, B. A. Diner, J. McCracken, S. Styring, Photosynth. Res. 1995, 46, 177.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsFejsA%3D%3D&md5=23458410386145259fbdecf747cdc221CAS |

[34] C. D. Delfs, R. Stranger, Inorg. Chem. 2003, 42, 2495.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitF2ru7w%3D&md5=01fcc169ab4dbcc491d1c78e313740d1CAS |

[35] G. C. Dismukes, R. Brimblecombe, G. A. N. Felton, R. S. Pryadun, J. E. Sheats, L. Spiccia, G. F. Swiegers, Acc. Chem. Res. 2009, 42, 1935.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVSgtb%2FL&md5=7ee1e63bbf20e924e0a4d165bd1f212dCAS |

[36] B. Cornell, G. Khrishna, P. Osman, R. Pace, L. Wieczorek, Biochem. Soc. Trans. 2001, 29, 613.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXms1SltLw%3D&md5=b7dc55aa2867b5d7345222206f58efddCAS |

[37] S. Y. Reece, J. A. Hamel, K. Sung, T. D. Jarvi, A. J. Esswein, J. J. H. Pijpers, D. G. Nocera, Science 2011, 334, 645.
| Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlyqu7vF&md5=e0298161b92e218b9b45c56538dc6eb5CAS |