Novel, oxygen-insensitive group 5 [NiFe]-hydrogenase in Ralstonia eutropha

Applied and Environmental Microbiology

Volumn 79, Issue 17, 2013, Pages 5137-5145

  Schäfer, Caspar ^a   Friedrich, Bärbel ^a   Lenza, Oliver ^b  

^a HUMBOLDT UNIVERSITY   (Germany)

^b TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY MEASUREMENTS; ATMOSPHERIC LEVELS; BIOCHEMICAL CHARACTERIZATION; MICHAELIS CONSTANTS; MOLECULAR HYDROGEN; NITROBLUE TETRAZOLIUM; OXIDATION ACTIVITIES; RALSTONIA EUTROPHA;

AFFINITY CHROMATOGRAPHY; BACTERIA; CHLORINE COMPOUNDS; OXYGEN;

ENZYME ACTIVITY;

BIOCHEMISTRY; CATALYSIS; CHROMATOGRAPHY; CONCENTRATION (COMPOSITION); ENZYME ACTIVITY; HOMOGENEITY; HYDROGEN; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; OXIDATION; SOIL MICROORGANISM;

EID: 84884237449     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01576-13     Document Type: Article

References (52)

1. Constant P, Poissant L, Villemur R. 2009. Tropospheric H2 budget and the response of its soil uptake under the changing environment. Sci. Total Environ. 407:1809-1823.
2. Thauer RK. 2011. Hydrogenases and the global H2 cycle. Eur. J. Inorg. Chem. 2011:919-921.
3. Guo RB, Conrad R. 2008. Extraction and characterization of soil hydrogenases oxidizing atmospheric hydrogen. Soil Biol. Biochem. 40:1149-1154.
4. Constant P, Poissant L, Villemur R. 2008. Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2. ISME J. 2:1066-1076.
5. Constant P, Chowdhury SP, Hesse L, Conrad R. 2011. Co-localization of atmospheric H2 oxidation activity and high affinity H2-oxidizing bacteria in non-axenic soil and sterile soil amended with Streptomyces sp. PCB7. Soil Biol. Biochem. 43:1888-1893.
6. Vignais PM, Billoud B. 2007. Occurrence, classification, and biological function of hydrogenases: an overview. Chem. Rev. 107:4206-4272.
7. Schwartz E, Fritsch J, Friedrich B. 2013. H2-metabolizing prokaryotes, p 119-199. In Rosenberg E, DeLong E, Lory S, Stackebrandt E, Thompson F (ed), The prokaryotes: prokaryotic physiology and biochemistry, 4th ed. Springer, Berlin, Germany.
8. Constant P, Chowdhury SP, Hesse L, Pratscher J, Conrad R. 2011. Genome data mining and soil survey for the novel group 5 [NiFe]-hydrogenase to explore the diversity and ecological importance of presumptive high-affinity H2-oxidizing bacteria. Appl. Environ. Microbiol. 77:6027-6035.
9. Böck A, King PW, Blokesch M, Posewitz MC. 2006. Maturation of hydrogenases. Adv. Microb. Physiol. 51:1-71.
10. Lenz O, Ludwig M, Schubert T, Bürstel I, Ganskow S, Goris T, Schwarze A, Friedrich B. 2010. H2 conversion in the presence of O2 as performed by the membrane-bound [NiFe]-hydrogenase of Ralstonia eutropha. Chem. Phys. Chem. 11:1107-1119.
11. Blokesch M, Paschos A, Theodoratou E, Bauer E, Hube M, Huth S, Böck A. 2002. Metal insertion into [NiFe]-hydrogenases. Biochem. Soc. Trans. 30:674-680.
12. Palmer T, Berks BC. 2012. The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10:483-496.
13. Berney M, Cook GM. 2010. Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 5:e8614. doi:10.1371/journal.pone.0008614.
14. Schwartz E, Henne A, Cramm R, Eitinger T, Friedrich B, Gottschalk G. 2003. Complete nucleotide sequence of pHG1: a Ralstonia eutropha H16 megaplasmid encoding key enzymes ofH2-based lithoautotrophy and anaerobiosis. J. Mol. Biol. 332:369-383.
15. Pohlmann A, Fricke WF, Reinecke F, Kusian B, Liesegang H, Cramm R, Eitinger T, Ewering C, Potter M, Schwartz E, Strittmatter A, Voss I, Gottschalk G, Steinbüchel A, Friedrich B, Bowien B. 2006. Genome sequence of the bioplastic-producing "Knallgas" bacterium Ralstonia eutropha H16. Nat. Biotechnol. 24:1257-1262.
16. Lenz O, Bernhard M, Buhrke T, Schwartz E, Friedrich B. 2002. The hydrogen-sensing apparatus in Ralstonia eutropha. J. Mol. Microbiol. Biotechnol. 4:255-262.
17. Burgdorf T, Löscher S, Liebisch P, Van der Linden E, Galander M, Lendzian F, Meyer-Klaucke W, Albracht SPJ, Friedrich B, Dau H, Haumann M. 2005. Structural and oxidation-state changes at its nonstandard [NiFe] site during activation of the NAD-reducing hydrogenase from Ralstonia eutropha detected by X-ray absorption, EPR, and FTIR spectroscopy. J. Am. Chem. Soc. 127:576-592.
18. Fritsch J, Lenz O, Friedrich B. 2013. Structure, function and biosynthesis of O2-tolerant hydrogenases. Nat. Rev. Microbiol. 11:106-114.
19. Yanisch-Perron C, Vieira J, Messing J. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
20. Simon R, Priefer U, Pühler A. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gramnegative bacteria. Biotechnology 1:784-791.
21. Lenz O, Schwartz E, Dernedde J, Eitinger M, Friedrich B. 1994. The Alcaligenes eutrophus H16 hoxX gene participates in hydrogenase regulation. J. Bacteriol. 176:4385-4393.
22. Goris T, Wait AF, Saggu M, Fritsch J, Heidary N, Stein M, Zebger I, Lendzian F, Armstrong FA, Friedrich B, Lenz O. 2011. A unique ironsulfur cluster is crucial for oxygen tolerance of a [NiFe]-hydrogenase. Nat. Chem. Biol. 7:310-318.
23. Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150: 76-85.
24. Schwartz E, Voigt B, Zühlke D, Pohlmann A, Lenz O, Albrecht D, Schwarze A, Kohlmann Y, Krause C, Hecker M, Friedrich B. 2009. A proteomic view of the facultatively chemolithoautotrophic lifestyle of Ralstonia eutropha H16. Proteomics 9:5132-5142.
25. Neumann M, Mittelstädt G, Seduk F, Iobbi-Nivol C, Leimkühler S. 2009. MocA is a specific cytidylyltransferase involved in molybdopterin cytosine dinucleotide biosynthesis in Escherichia coli. J. Biol. Chem. 284: 21891-21898.
26. Kleihues L, Lenz O, Bernhard M, Buhrke T, Friedrich B. 2000. The H2 sensor of Ralstonia eutropha is a member of the subclass of regulatory [NiFe] hydrogenases. J. Bacteriol. 182:2716-2724.
27. Wang R, Healey FP, Myers J. 1971. Amperometric measurement of hydrogen evolution in Chlamydomonas. Plant Physiol. 48:108-112.
28. Kohlmann Y, Pohlmann A, Otto A, Becher D, Cramm R, Lütte S, Schwartz E, Hecker M, Friedrich B. 2011. Analyses of soluble and membrane proteomes of Ralstonia eutropha H16 reveal major changes in the protein complement in adaptation to lithoautotrophy. J. Proteome Res. 10:2767-2776.
29. Ludwig M, Cracknell JA, Vincent KA, Armstrong FA, Lenz O. 2009. Oxygen-tolerantH2 oxidation by membrane-bound [NiFe] hydrogenases of Ralstonia species: coping with low level H2 in air. J. Biol. Chem. 284: 465-477.
30. Jones A, Lenz O, Strack A, Buhrke T, Friedrich B. 2004. [NiFe] hydrogenase active site biosynthesis: identification of Hyp protein complexes in Ralstonia eutropha. Biochemistry 43:13467-13477.
31. Wilde E. 1962. Untersuchungen über Wachstum und Speicherstoffsynthese von Hydrogenomonas. Archiv. Mikrobiol. 43:109-137.
32. Cracknell JA, Wait AF, Lenz O, Friedrich B, Armstrong FA. 2009. A kinetic and thermodynamic understanding of O2 tolerance in [NiFe]-hydrogenases. Proc. Natl. Acad. Sci. U. S. A. 106:20681-20686.
33. Lauterbach L, Lenz O, Vincent KA. 2013. H2-driven cofactor regeneration using NAD(P)-reducing hydrogenases. FEBS J. 280:3058-3068.
34. Buhrke T, Lenz O, Porthun A, Friedrich B. 2004. The H2-sensing complex of Ralstonia eutropha: interaction between a regulatory [NiFe] hydrogenase and a histidine protein kinase. Mol. Microbiol. 51:1677-1689.
35. Pinske C, Jaroschinsky M, Sargent F, Sawers G. 2012. Zymographic differentiation of [NiFe]-hydrogenases 1, 2, and 3 of Escherichia coli K-12. BMC Microbiol. 12:134.
36. Liochev S, Hausladen A, Beyer W, Fridovich I. 1994. NADPH: ferredoxin oxidoreductase acts as a paraquat diaphorase and is a member of the soxRS regulon. Proc. Natl. Acad. Sci. U. S. A. 91:1328-1331.
37. Brown DM, Upcroft JA, Upcroft P. 1996. A H2O-producing NADH oxidase from the protozoan parasite Giardia duodenalis. Eur. J. Biochem. 241:155-161.
38. Schreiner ME, Eikmanns BJ. 2005. Pyruvate: quinone oxidoreductase from Corynebacterium glutamicum-purification and biochemical characterization. J. Bacteriol. 187:862-871.
39. Niraula NP, Shrestha P, Oh TJ, Sohng JK. 2010. Identification and characterization of a NADH oxidoreductase involved in phenylacetic acid degradation pathway from Streptomyces peucetius. Microbiol. Res. 165: 649-656.
40. Michal G, Möllering H, Siedel J. 1983. Chemical design for indicator reactions in the visible range, p 197-232. In BergmeyerH-U(ed), Methods of enzymatic analysis, 3rd ed, vol 1. Verlag Chemie, Weinheim, Germany.
41. Schneider K, Schlegel HG. 1976. Purification and properties of soluble hydrogenase from Alcaligenes eutrophus H 16. Biochim. Biophys. Acta 452:66-80.
42. Hedderich R, Albracht SP, Linder D, Koch J, Thauer RK. 1992. Isolation and characterization of polyferredoxin from Methanobacterium thermoautotrophicum: the mvhB gene product of the methylviologenreducing hydrogenase operon. FEBS Lett. 298:65-68.
43. Calzolai L Gorst CM, Zhao ZH, Teng Q, Adams MW, La Mar GN. 1995. 1H-NMR investigation of the electronic and molecular structure of the four-iron cluster ferredoxin from the hyperthermophile Pyrococcus furiosus: identification of Asp14 as a cluster ligand in each of the four redox states. Biochemistry 34:11373-11384.
44. Gruner I, Frädrich C, Böttger LH, Trautwein AX, Jahn D, Härtig E. 2011. Aspartate 141 is the fourth ligand of the oxygen-sensing [4Fe-4S]2+ cluster of Bacillus subtilis transcriptional regulator Fnr. J. Biol. Chem. 286:2017-2021.
45. Dernedde J, Eitinger T, Patenge N, Friedrich B. 1996. hyp gene products in Alcaligenes eutrophus are part of a hydrogenase-maturation system. Eur. J. Biochem. 235:351-358.
46. Wolf I, Buhrke T, Dernedde J, Pohlmann A, Friedrich B. 1998. Duplication of hyp genes involved in maturation of [NiFe] hydrogenases in Alcaligenes eutrophus H16. Arch. Microbiol. 170:451-459.
47. 2O, and NO). Microbiol. Rev. 60:609-640.
48. Constant P, Chowdhury SP, Pratscher J, Conrad R. 2010. Streptomycetes contributing to atmospheric molecular hydrogen soil uptake are widespread and encode a putative high-affinity [NiFe]-hydrogenase. Environ. Microbiol. 12:821-829.
49. Conrad R, Aragno M, Seiler W. 1983. The inability of hydrogen bacteria to utilize atmospheric hydrogen is due to threshold and affinity for hydrogen. FEMS Microbiol. Lett. 18:207-210.
50. Fritsch J, Scheerer P, Frielingsdorf S, Kroschinsky S, Friedrich B, Lenz O, Spahn CMT. 2011. The crystal structure of an oxygen-tolerant hydrogenase uncovers a novel iron-sulphur centre. Nature 479:249-252.
51. Massanz C, Fernandez VM, Friedrich B. 1997. C-terminal extension of the H2-activating subunit, HoxH, directs maturation of the NADreducing hydrogenase in Alcaligenes eutrophus. Eur. J. Biochem. 245:441-448.
52. Buhrke T. 2002. Der H2-Sensor von Ralstonia eutropha: Struktur-Funktions-Beziehungen einer Neuartigen [NiFe]-Hydrogenase. Ph.D. thesis. Humboldt-Universität zu Berlin, Berlin, Germany. Properties of a Group 5 [NiFe]-Hydrogenase September