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Structural Foundations for O2 Sensitivity and O2 Tolerance in [NiFe]-Hydrogenases

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Book cover Microbial BioEnergy: Hydrogen Production

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 38))

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Summary

Nature has evolved three different ways of metabolizing hydrogen, represented by the anaerobic [Fe]-, [FeFe]- and [NiFe]-hydrogenases. Structural and functional studies of these enzymes have unveiled the unusual composition of their active sites and characterized their catalytic mechanisms. From a biotechnological viewpoint, the most interesting hydrogenases are those that contain a [NiFe] moiety in their active sites. Some of these enzymes are O2-resistant and can rapidly reductively recover from oxygen exposure whereas others are O2-tolerant and can oxidize H2 even at atmospheric oxygen levels. O2-resistant [NiFeSe]-hydrogenases have one of the Cys ligands of the active site replaced by a SeCys and do not display the hard-to-reactivate “unready” state provoked by O2. The reasons for this property might be related to the formation of O2-derived Se-O bonds, which are weaker than S-O bonds and, consequently, easier to break upon reduction. Conversely, membrane-bound O2-tolerant hydrogenases have an unusual proximal (relative to the active site) [Fe4S3] cluster coordinated by six Cys ligands. This cluster can rapidly send two successive electrons to the active site helping to reduce oxygen to water there. Some microorganisms posses more than one hydrogenase and use them in different ways. For instance, there are three well-characterized [NiFe]-hydrogenases in the model bacterium Escherichia coli. They are highly regulated and each one plays a specific role: microaerobic/anaerobic H2 uptake, anaerobic H2 evolution and, protection from O2-induced damage, respectively. These enzymes are discussed in connection with the metabolic changes E. coli undergoes during its transit through the intestinal tract of the host. O2-tolerant hydrogenases have been used to build bio-fuel cells that can function under air. Also, O2-resistant [NiFeSe]-hydrogenases have been attached to TiO2 particules for H2 production from solar energy. Hydrogenase active sites have also served as a source of inspiration for the synthesis of organometallic catalysts.

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Abbreviations

EPR –:

Electron Paramagnetic Resonance spectroscopy;

FTIR –:

Fourier Transform InfraRed spectroscopy;

Pt –:

Platinum;

TiO2 – :

Titanium dioxide

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Acknowledgements

The authors thank the Commissariat à l’Energie Atomique et aux Energies Alternatives (CEA) and the Centre National de la Recherche Scientifique (CNRS) for institutional funding and the Agence Nationale de la Recherche for several contracts concerning the subject of this chapter. Erwin Reisner is thanked for providing Fig. 2.5b.

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  1. Metalloproteins Unit, Institut de Biologie Structurale J.P. Ebel, Commissariat à l’Énergie Atomique, Centre National de la Recherche Scientifique, Université Joseph Fourier, UMR 5075, 41 rue Jules Horowitz, 38027, Grenoble, France

    Anne Volbeda & Juan C. Fontecilla-Camps

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Correspondence to Juan C. Fontecilla-Camps .

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  1. Dept. of Pharmacy and BioTechnology, University of Bologna, Bologna, Italy

    Davide Zannoni

  2. Dept. of AgriFood Production and Environmental Sciences, University of Florence, Florence, Italy

    Roberto De Philippis

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© 2014 Springer Science+Business Media Dordrecht

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Volbeda, A., Fontecilla-Camps, J.C. (2014). Structural Foundations for O2 Sensitivity and O2 Tolerance in [NiFe]-Hydrogenases. In: Zannoni, D., De Philippis, R. (eds) Microbial BioEnergy: Hydrogen Production. Advances in Photosynthesis and Respiration, vol 38. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-8554-9_2

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