Site Saturation Mutagenesis Demonstrates a Central Role for Cysteine 298 as Proton Donor to the Catalytic Site in CaHydA [FeFe]-Hydrogenase

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Morra, Simone ^a   Giraudo, Alberto ^a   Di Nardo, Giovanna ^a   King, Paul W ^b   Gilardi, Gianfranco ^a   Valetti, Francesca ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b NATIONAL RENEWABLE ENERGY LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; CYSTEINE; HYDROGEN; IRON; IRON HYDROGENASE; OXYGEN;

AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CLOSTRIDIUM ACETOBUTYLICUM; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME METABOLISM; GENE MUTATION; MUTAGENESIS; MUTANT; NONHUMAN; PH; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTON TRANSPORT; SITE SATURATION MUTAGENESIS;

ASPARTIC ACID; CATALYTIC DOMAIN; CLOSTRIDIUM ACETOBUTYLICUM; CODON; CYSTEINE; DNA; ESCHERICHIA COLI; GENE LIBRARY; HYDROGEN; HYDROGEN BONDING; HYDROGEN-ION CONCENTRATION; HYDROGENASE; IRON-SULFUR PROTEINS; KINETICS; MUTAGENESIS; OXIDATION-REDUCTION; OXYGEN; PLASMIDS; PROTEIN STRUCTURE, TERTIARY; PROTONS;

EID: 84868089020     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048400     Document Type: Article

References (43)

1. Adams MWW, (1990) The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1020: 115-145.
2. Vignais PM, Billoud P, (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107: 4206-4272.
3. Hallenbeck PC, (2009) Fermentative hydrogen production: principles, progress, and prognosis. Int J Hydrogen Energy 34: 7379-7389.
4. McKinlay JB, Harwood CS, (2010) Photobiological production of hydrogen gas as a biofuel. Curr Opin Biotechnol 21: 244-251.
5. Cracknell JA, Vincent KA, Armstrong FA, (2008) Enzymes as working or inspirational electrocatalysts for fuel cells and electrolysis. Chem Rev 108: 2439-2461.
6. Hambourger M, Gervaldo M, Svedruzic D, King PW, Gust D, et al. (2008) [FeFe]-hydrogenase-catalyzed H2 production in a photoelectrochemical biofuel cell. J Am Chem Soc 130: 2015-2022.
7. Armstrong FA, Belsey NA, Cracknell JA, Goldet G, Parkin A, et al. (2009) Dynamic electrochemical investigations of hydrogen oxidation and production by enzymes and implications for future technology. Chem Soc Rev 38: 36-51.
8. Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y, (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107: 4273-4303.
9. Meyer J, (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64: 1063-1084.
10. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC, (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom resolution. Science 282: 1853-1858.
11. Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC, (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7: 13-23.
12. Pandey AS, Harris TV, Giles LJ, Peters JW, Szilagyi RK, (2008) Dithiomethylether as a ligand in the hydrogenase H-Cluster. J Am Chem Soc 130: 4533-4540.
13. Silakov A, Wenk B, Reijerse E, Lubitz W, (2009) 14N HYSCORE investigation of the H-cluster of [FeFe] hydrogenase evidence for a nitrogen in the dithiol bridge. Phys Chem Chem Phys 11: 6592-6599.
14. Nicolet Y, Fontecilla-Camps JC, Fontecave M, (2010) Maturation of [FeFe]-hydrogenases: Structures and mechanisms. Int J Hydrogen Energy 35: 10750-10760.
15. Mulder DW, Shepard EM, Meuser JE, Joshi N, King PW, et al. (2011) Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydAΔEFG. Structure 19: 1038-1052.
16. De Lacey AL, Fernández VM, (2007) Activation and inactivation of hydrogenase function and the catalytic cycle: spectroelectrochemical studies. Chem Rev 107: 4304-4330.
17. Lubitz W, Reijerse E, van Gastel M, (2007) [NiFe] and [FeFe] Hydrogenases Studied by Advanced Magnetic Resonance Techniques. Chem Rev 107: 4331-4365.
18. Fontecilla-Camps JC, Amara P, Cavazza C, Nicolet Y, Volbeda A, (2009) Structure-function relationships of anaerobic gas-processing metalloenzymes. Nature 460: 814-822.
19. Knörzer P, Silakov A, Foster CE, Armstrong FA, Lubitz W, et al. (2012) Importance of the Protein Framework for Catalytic Activity of [FeFe]-Hydrogenases. J Biol Chem 286: 38341-38347.
20. Nicolet Y, Lemon BJ, Fontecilla-Camps JC, Peters JW, (2000) A novel FeS cluster in Fe-only hydrogenases. Trends Biochem Sci 25: 138-143.
21. Greco C, Bruschi M, De Gioia L, Ryde U, (2007) A QM/MM Investigation of the Activation and Catalytic Mechanism of Fe-Only Hydrogenases. Inorg Chem 46: 5911-5921.
22. Hong G, Cornish AJ, Hegg EL, Pachter R, (2011) On understanding proton transfer to the biocatalytic [Fe-Fe]H sub-cluster in [Fe-Fe] H2ases: QM/MM MD simulations. Biochim Biophys Acta 1807: 510-517.
23. Lautier T, Ezanno P, Baffert C, Fourmond V, Cournac L, et al. (2011) The quest for a functional substrate access tunnel in FeFe hydrogenase. Faraday Discuss 148: 385-407.
24. Cornish AJ, Gärtner K, Yang H, Peters JW, Hegg EL, (2011) Mechanism of Proton Transfer in [FeFe]-Hydrogenase from Clostridium pasteurianum. J Biol Chem 286: 38341-38347.
25. Chica RA, Doucet N, Pelletier JN, (2005) Semi-rational approaches to engineering enzyme activity: combining the benefits of directed evolution and rational design. Curr Opin Biotechnol 16: 378-384.
26. Reetz MT, Carballeira JD, (2007) Iterative saturation mutagenesis (ISM) for rapid directed evolution of functional enzymes. Nat Protoc 2: 891-903.
27. Patrick WM, Firth AE, Blackburn JM, (2003) User-friendly algorithms for estimating completeness and diversity in randomized protein-encoding libraries. Protein Eng 16: 451-457.
28. Dixon M, Webb EC (1979) Enzymes, 3rd ed. New York: Academic Press.
29. Cleland WW, (1982) The use of pH studies to determine chemical mechanisms of enzyme-catalyzed reactions. Methods Enzymol 87: 390-405.
30. Multani JS, Mortenson LE, (1972) Circular dichroism spectra of hydrogenase from Clostridium pasteurianum W5. Biochim Biophys Acta 256: 66-70.
31. Stapleton JA, Swartz JR, (2010) A Cell-Free Microtiter Plate Screen for Improved [FeFe] Hydrogenases. PLoS ONE 5: e10554.
32. Stapleton JA, Swartz JR, (2010) Development of an In Vitro Compartmentalization Screen for High-Throughput Directed Evolution of [FeFe] Hydrogenases. PLoS ONE 5: e15275.
33. Bingham AS, Smith PR, Swartz JR, (2012) Evolution of an [FeFe] hydrogenase with decreased oxygen sensitivity. Int J Hydrogen Energy 37: 2965-2976.
34. Gunner MR, Mao J, Song Y, Kim J, (2006) Factors influencing the energetics of electron and proton transfers in proteins. What can be learned from calculations? Biochim Biophys Acta 1757: 942-968.
35. Cukierman S, (2006) Et tu, Grotthuss! and other unfinished stories. Biochim Biophys Acta 1757: 876-885.
36. Dementin S, Burlat B, De Lacey AL, Pardo A, Adryanczyk-Perrier G, et al. (2004) A Glutamate Is the Essential Proton Transfer Gate during the Catalytic Cycle of the [NiFe] Hydrogenase. J Biol Chem 279: 10508-10513.
37. Cohen J, Kim K, King P, Seibert M, Schulten K, (2005) Finding gas diffusion pathways in proteins: application to O2 and H2 transport in CpI [FeFe]-hydrogenase and the role of packing defects. Structure 13: 1321-1329.
38. Goldet G, Brandmayr C, Stripp ST, Happe T, Cavazza C, et al. (2009) Electrochemical Kinetic Investigations of the Reactions of [FeFe]-Hydrogenases with Carbon Monoxide and Oxygen: Comparing the Importance of Gas Tunnels and Active-Site Electronic/Redox Effects. J Am Chem Soc 131: 14979-14989.
39. Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, et al. (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. PNAS 106: 17331-17336.
40. Lambertz C, Leidel N, Havelius KGV, Noth J, Chernev P, et al. (2011) O2 Reactions at the Six-iron Active Site (H-cluster) in [FeFe]-Hydrogenase. J Biol Chem 286: 40614-40623.
41. Pace CN, Grimsley GR, Scholtz JM, (2009) Protein Ionizable Groups: pK Values and Their Contribution to Protein Stability and Solubility. J Biol Chem 284: 13285-13289.
42. King PW, Posewitz MC, Ghirardi ML, Seibert M, (2006) Functional studies of [FeFe] hydrogenase maturation in an Escherichia coli biosynthetic system. J Bacteriol 188: 2163-2172.
43. Adams MWW, Mortenson LE, (1984) The physical and catalytic properties of hydrogenase II of Clostridium pasteurianum. J Biol Chem 259: 7045-7055.