A broad survey reveals substitution tolerance of residues ligating FeS clusters in [NiFe] hydrogenase

BMC Biochemistry

Volumn 15, Issue 1, 2014, Pages

  Yonemoto, Isaac T ^a   Clarkson, Benjamin R ^a   Smith, Hamilton O ^a   Weyman, Philip D ^a  

^a J CRAIG VENTER INSTITUTE   (United States)

Author keywords

Alteromonas macleodii deep ecotype; Iron sulfur cluster; NiFe hydrogenase

Indexed keywords

ASPARAGINE; ASPARTIC ACID; CYSTEINE; FERREDOXIN; GLUTAMINE; HISTIDINE; HYDROGENASE; BACTERIAL PROTEIN; BIOFUEL; HYDROGEN; IRON; NICKEL-IRON HYDROGENASE; SULFUR DERIVATIVE;

ALTEROMONAS; ALTEROMONAS MACLEODII; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ECOTYPE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; GENETIC SCREENING; HYDROGEN EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATION REDUCTION POTENTIAL; PHOTOSYNTHESIS; REVIEW; SEQUENCE DATABASE; WHOLE CELL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; METABOLISM; PROCEDURES; SITE DIRECTED MUTAGENESIS;

ALTEROMONAS MACLEODII 'DEEP ECOTYPE';

ALTEROMONAS; AMINO ACID SUBSTITUTION; ASPARTIC ACID; BACTERIAL PROTEINS; BIOFUELS; HYDROGEN; HYDROGENASE; IRON; MOLECULAR STRUCTURE; MUTAGENESIS, SITE-DIRECTED; PHOTOSYNTHESIS; SULFUR COMPOUNDS;

EID: 84902301756     PISSN: None     EISSN: 14712091     Source Type: Journal    
DOI: 10.1186/1471-2091-15-10     Document Type: Review

References (33)

1. The oxygen sensitivity of nitrogenase: a problem for biochemists and micro-organisms. Gallon JR, Trends Biochem Sci 1981 6 19 23
2. Evolution of an [FeFe] hydrogenase with decreased oxygen sensitivity. Bingham AS, Smith PR, Swartz JR, Int J Hydrog Energy 2012 37 2965 2976 10.1016/j.ijhydene.2011.02.048
3. How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, Haumann M, Armstrong FA, Happe T, Proc Natl Acad Sci 2009 106 17331 17336 10.1073/pnas.0905343106 19805068
4. [NiFe] hydrogenase from alteromonas macleodii with unusual stability in the presence of oxygen and high temperature. Vargas WA, Weyman PD, Tong Y, Smith HO, Xu Q, Appl Environ Microbiol 2011 77 1990 1998 10.1128/AEM.01559-10 21257809
5. Isolation and characterization of the small subunit of the uptake hydrogenase from the cyanobacterium nostoc punctiforme. Raleiras P, Kellers P, Lindblad P, Styring S, Magnuson A, J Biol Chem 2013 288 18345 18352 10.1074/jbc.M113.468587 23649626
6. Heterologous expression of alteromonas macleodii and thiocapsa roseopersicina [NiFe] hydrogenases in synechococcus elongatus. Weyman PD, Vargas WA, Tong Y, Yu J, Maness P-C, Smith HO, Xu Q, PLoS One 2011 6 20126 10.1371/journal.pone.0020126 21637846
7. Heterologous expression of alteromonas macleodii and thiocapsa roseopersicina [NiFe] hydrogenases in Escherichia coli. Weyman PD, Vargas WA, Chuang R-Y, Chang Y, Smith HO, Xu Q, Microbiology 2011 157 1363 1374 10.1099/mic.0.044834-0 21349975
8. Dual organism design cycle reveals small subunit substitutions that improve [NiFe] hydrogenase hydrogen evolution. Yonemoto IT, Matteri CW, Nguyen TA, Smith HO, Weyman PD, J Biol Eng 2013 7 17 10.1186/1754-1611-7-17 23819621
9. A serine → cysteine ligand mutation in the high potential iron-sulfur protein from chromatium vinosum provides insight into the electronic structure of the [4Fe-4S] cluster. Babini E, Bertini I, Borsari M, Capozzi F, Dikiy A, Eltis LD, Luchinat C, J Am Chem Soc 1996 118 75 80 10.1021/ja952636+ (Pubitemid 3017422)
10. Modified ligands to FA and Fb in photosystem I I. Structural constraints for the formation of iron-sulfur clusters in free and rebound PsaC. Mehari T, Qiao F, Scott MP, Nellis DF, Zhao J, Bryant DA, Golbeck JH, J Biol Chem 1995 270 28108 28117 10.1074/jbc.270.47.28108 7499299 (Pubitemid 3016541)
11. In Azotobacter vinelandii hydrogenase, substitution of serine for the cysteine residues at positions 62, 65, 294, and 297 in the small (HoxK) subunit affects H2 oxidation. Sayavedra-Soto LA, Arp DJ, J Bacteriol 1993 175 3414 3421 8501046 (Pubitemid 23163385)
12. Effect of serinate ligation at each of the iron sites of the [Fe4S4] cluster of pyrococcus furiosus ferredoxin on the redox, spectroscopic, and biological properties. Brereton PS, Duderstadt RE, Staples CR, Johnson MK, Adams MWW, Biochemistry 1999 38 10594 10605 10.1021/bi990671d 10441157 (Pubitemid 29383433)
13. Site-directed mutagenesis of the cysteine ligands to the [4Fe-4S] cluster of Escherichia coli MutY. Golinelli M-P, Chmiel NH, David SS, Biochemistry 1999 38 6997 7007 10.1021/bi982300n 10353811 (Pubitemid 29262761)
14. Alternative FeS cluster ligands: tuning redox potentials and chemistry. Bak DW, Elliott SJ, Curr Opin Chem Biol 2014 19 50 58 24463764
15. Electron transfer in proteins. Gray HB, Winkler JR, Annu Rev Biochem 1996 65 537 561 10.1146/annurev.bi.65.070196.002541 8811189 (Pubitemid 26250619)
16. Crystal structure of the nickel-iron hydrogenase from desulfovibrio gigas. Volbeda A, Charon M-H, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC, Nature 1995 373 580 587 10.1038/373580a0 7854413
17. [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [NiFe] hydrogenase by site-directed mutagenesis. Rousset M, Montet Y, Guigliarelli B, Forget N, Asso M, Bertrand P, Fontecilla-Camps JC, Hatchikian EC, Proc Natl Acad Sci 1998 95 11625 11630 10.1073/pnas.95.20.11625 9751716 (Pubitemid 28460465)
18. Spectroscopic characterization of the novel iron-sulfur cluster in Pyrococcus furiosus ferredoxin. Conover RC, Kowal AT, Fu WG, Park JB, Aono S, Adams MW, Johnson MK, J Biol Chem 1990 265 8533 8541 2160461
19. Electrochemical and spectroscopic characterization of the 7Fe form of ferredoxin III from Desulfovibrio africanus. Armstrong FA, George SJ, Cammack R, Hatchikian EC, Thomson AJ, Biochem J 1989 264 265 273 2557831 (Pubitemid 19283527)
20. [3Fe-4S]↔[4Fe-4S] cluster interconversion in desulfovibrio africanus ferredoxin III: properties of an Asp14 → Cys mutant. Busch J, Breton J, Bartlett B, Armstrong F, James R, Thomson A, Biochem J 1997 323 95 102 9173907
21. Characterization of the [3Fe-4S] and [4Fe-4S] clusters in unbound PsaC mutants C14D and C51D. Midpoint potentials of the single [4Fe-4S] clusters are identical to FA and FB in bound PsaC of photosystem I. Yu L, Zhao J, Lu W, Bryant DA, Golbeck JH, Biochemistry 1993 32 8251 8258 10.1021/bi00083a028 8394132 (Pubitemid 23265817)
22. Evidence for a mixed-ligand [4Fe-4S] cluster in the C14D mutant of PsaC. Altered reduction potentials and EPR spectral properties of the FA and FB clusters on rebinding to the P700-FX core. Yu L, Bryant DA, Golbeck JH, Biochemistry 1995 34 7861 7868 10.1021/bi00024a010 7794897
23. Ferredoxin has a pivotal role in the biosynthesis of the hydrogen-oxidizing hydrogenases in Escherichia coli. Jaroschinsky M, Sawers RG, Int J Hydrog Energy 2014 In Press
24. Hyperproduction of recombinant ferredoxins in Escherichia coli by coexpression of the ORF1-ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster. Nakamura M, Saeki K, Takahashi Y, J Biochem 1999 126 10 18 10.1093/ oxfordjournals.jbchem.a022409 10393315 (Pubitemid 29355387)
25. Transforming an oxygen-tolerant [NiFe] uptake hydrogenase into a proficient, reversible hydrogen producer. Murphy BJ, Sargent F, Armstrong FA, Energy Environ Sci 2014 7 1426 1433 10.1039/c3ee43652g
26. Oxygen-tolerant [NiFe]-hydrogenases: the individual and collective importance of supernumerary cysteines at the proximal Fe-S cluster. Lukey MJ, Roessler MM, Parkin A, Evans RM, Davies RA, Lenz O, Friedrich B, Sargent F, Armstrong FA, J Am Chem Soc 2011 133 16881 16892 10.1021/ja205393w 21916508
27. A unique iron-sulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Goris T, Wait AF, Saggu M, Fritsch J, Heidary N, Stein M, Zebger I, Lendzian F, Armstrong FA, Friedrich B, Lenz O, Nat Chem Biol 2011 7 310 318 10.1038/nchembio.555 21390036
28. Structural basis for a [4Fe-3S] cluster in the oxygen-tolerant membrane-bound [NiFe]-hydrogenase. Shomura Y, Yoon K-S, Nishihara H, Higuchi Y, Nature 2011 479 253 256 10.1038/nature10504 22002607
29. Biogeography of the ubiquitous marine bacterium Alteromonas macleodii determined by multilocus sequence analysis. Ivars-Martínez E, D'Auria G, RodríGuez-Valera F, SáNchez-Porro C, Ventosa A, Joint I, MüHling M, Mol Ecol 2008 17 4092 4106 10.1111/j.1365-294X.2008.03883.x 19238708
30. The strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Schmidt TG, Skerra A, Nat Protoc 2007 2 1528 1535 10.1038/nprot.2007.209 17571060 (Pubitemid 46952331)
31. Mutagenesis of a flexible loop in streptavidin leads to higher affinity for the strep-tag II peptide and improved performance in recombinant protein purification. Voss S, Skerra A, Protein Eng 1997 10 975 982 10.1093/protein/10. 8.975 9415448 (Pubitemid 27491655)
32. Engineering a non-native hydrogen production pathway into Escherichia coli via a cyanobacterial [NiFe] hydrogenase. Wells MA, Mercer J, Mott RA, Pereira-Medrano AG, Burja AM, Radianingtyas H, Wright PC, Metab Eng 2011 13 445 453 10.1016/j.ymben.2011.01.004 21276867
33. Protein production by auto-induction in high-density shaking cultures. Studier FW, Protein Expr Purif 2005 41 207 234 10.1016/j.pep.2005.01.016 15915565