1887

Microbiology Society logo

Volume 161, Issue 11

Heterologous complementation studies in with the Hyp accessory protein machinery from provide insight into [NiFe]-hydrogenase large subunit recognition by the HypC protein family Free

Abstract

Six Hyp maturation proteins (HypABCDEF) are conserved in micro-organisms that synthesize [NiFe]-hydrogenases (Hyd). Of these, the HypC chaperones interact directly with the apo-form of the catalytically active large subunit of Hyd enzymes and are believed to transfer the Fe(CN)CO moiety of the bimetallic cofactor from the Hyp machinery to this large subunit. In HypC is specifically required for maturation of Hyd-3 while its paralogue, HybG, is specifically required for Hyd-2 maturation; either HypC or HybG can mature Hyd-1. In this study, we demonstrate that the products of the operon from the deeply branching hydrogen-dependent and obligate organohalide-respiring bacterium strain CBDB1 were capable of maturing and assembling active Hyd-1, Hyd-2 and Hyd-3 in an mutant. Maturation of Hyd-1 was less efficient, presumably because HypB of was necessary to restore optimal enzyme activity. In a reciprocal maturation study, the highly O-sensitive H-uptake HupLS [NiFe]-hydrogenase from CBDB1 was also synthesized in an active form in . Together, these findings indicated that HypC from CBDB1 exhibits promiscuity in its large subunit interaction in . Based on these findings, we generated amino acid variants of HybG capable of partial recovery of Hyd-3-dependent H production in a double null mutant. Together, these findings identify amino acid regions in HypC accessory proteins that specify interaction with the large subunits of hydrogenase and demonstrate functional compatibility of Hyp accessory protein machineries.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© 2015 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000177
2015-11-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/161/11/2204.html?itemId=/content/journal/micro/10.1099/mic.0.000177&mimeType=html&fmt=ahah

References

  1. Adrian L., Manz W., Szewzyk U., Görisch H. (1998). Physiological characterization of a bacterial consortium reductively dechlorinating 1,2,3- and 1,2,4-trichlorobenzeneAppl Environ Microbiol 64496–503[PubMed]. [Google Scholar]
  2. Albareda M., Manyani H., Imperial J., Brito B., Ruiz-Argüeso T., Böck A., Palacios J.M. (2012). Dual role of HupF in the biosynthesis of [NiFe] hydrogenase in Rhizobium leguminosarum BMC Microbiol 12256 [View Article][PubMed]. [Google Scholar]
  3. Albareda M., Pacios L.F., Manyani H., Rey L., Brito B., Imperial J., Ruiz-Argüeso T., Palacios J.M. (2014). Maturation of Rhizobium leguminosarum hydrogenase in the presence of oxygen requires the interaction of the chaperone HypC and the scaffolding protein HupKJ Biol Chem 28921217–21229 [View Article][PubMed]. [Google Scholar]
  4. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K., Tomita M., Wanner B., Mori H. (2006). Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collectionMol Syst Biol 22006.0008.[CrossRef] [Google Scholar]
  5. Ballantine S.P., Boxer D.H. (1985). Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12J Bacteriol 163454–459[PubMed]. [Google Scholar]
  6. Begg Y., Whyte J., Haddock B.A. (1977). The identification of mutants of Escherichia coli deficient in formate dehydrogenase and nitrate reductase activities using dye indicator platesFEMS Microbiol Lett 247–50 [View Article]. [Google Scholar]
  7. Blokesch M., Magalon A., Böck A. (2001). Interplay between the specific chaperone-like proteins HybG and HypC in maturation of hydrogenases 1, 2, and 3 from Escherichia coli J Bacteriol 1832817–2822 [View Article][PubMed]. [Google Scholar]
  8. Blokesch M., Paschos A., Theodoratou E., Bauer A., Hube M., Huth S., Böck A. (2002). Metal insertion into NiFe-hydrogenasesBiochem Soc Trans 30674–680 [View Article][PubMed]. [Google Scholar]
  9. Blokesch M., Albracht S.P.J., Matzanke B.F., Drapal N.M., Jacobi A., Böck A. (2004). The complex between hydrogenase-maturation proteins HypC and HypD is an intermediate in the supply of cyanide to the active site iron of [NiFe]-hydrogenasesJ Mol Biol 344155–167 [View Article][PubMed]. [Google Scholar]
  10. Böck A., King P.W., Blokesch M., Posewitz M.C. (2006). Maturation of hydrogenasesAdv Microb Physiol 511–71 [View Article][PubMed]. [Google Scholar]
  11. Bürstel I., Siebert E., Winter G., Hummel P., Zebger I., Friedrich B., Lenz O. (2012). A universal scaffold for synthesis of the Fe(CN)2(CO) moiety of [NiFe] hydrogenaseJ Biol Chem 28738845–38853 [View Article][PubMed]. [Google Scholar]
  12. Casadaban M.J. (1976). Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and MuJ Mol Biol 104541–555 [View Article][PubMed]. [Google Scholar]
  13. Cherepanov P.P., Wackernagel W. (1995). Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinantGene 1589–14 [View Article][PubMed]. [Google Scholar]
  14. Chung C.T., Niemela S.L., Miller R.H. (1989). One-step preparation of competent Escherichia coli: transformation and storage of bacterial cells in the same solutionProc Natl Acad Sci U S A 862172–2175 [View Article][PubMed]. [Google Scholar]
  15. Drapal N., Böck A. (1998). Interaction of the hydrogenase accessory protein HypC with HycE, the large subunit of Escherichia coli hydrogenase 3 during enzyme maturationBiochemistry 372941–2948 [View Article][PubMed]. [Google Scholar]
  16. Dubini A., Pye R.L., Jack R.L., Palmer T., Sargent F. (2002). How bacteria get energy from hydrogen: a genetic analysis of periplasmic hydrogen oxidation in Escherichia coli Int J Hydrogen Energy 271413–1420 [View Article]. [Google Scholar]
  17. Forzi L., Sawers R.G. (2007). Maturation of [NiFe]-hydrogenases in Escherichia coli Biometals 20565–578 [View Article][PubMed]. [Google Scholar]
  18. Holliger C., Schraa G., Stams A.J.M., Zehnder A.J.B. (1992). Enrichment and properties of an anaerobic mixed culture reductively dechlorinating 1,2,3-trichlorobenzene to 1,3-dichlorobenzeneAppl Environ Microbiol 581636–1644[PubMed]. [Google Scholar]
  19. Hormann K., Andreesen J.R. (1989). Reductive cleavage of sarcosine and betaine by Eubaterium acidaminophilum via enzyme systems different from glycine reductaseArch Microbiol 15350–59 [View Article]. [Google Scholar]
  20. Hube M., Blokesch M., Böck A. (2002). Network of hydrogenase maturation in Escherichia coli: role of accessory proteins HypA and HybFJ Bacteriol 1843879–3885 [View Article][PubMed]. [Google Scholar]
  21. Jack R.L., Buchanan G., Dubini A., Hatzixanthis K., Palmer T., Sargent F. (2004). Coordinating assembly and export of complex bacterial proteinsEMBO J 233962–3972 [View Article][PubMed]. [Google Scholar]
  22. Jacobi A., Rossmann R., Böck A. (1992). The hyp operon gene products are required for the maturation of catalytically active hydrogenase isoenzymes in Escherichia coli Arch Microbiol 158444–451 [View Article][PubMed]. [Google Scholar]
  23. Jayachandran G., Görisch H., Adrian L. (2004). Studies on hydrogenase activity and chlorobenzene respiration in Dehalococcoides sp. strain CBDB1Arch Microbiol 182498–504 [View Article][PubMed]. [Google Scholar]
  24. Jehmlich N., Schmidt F., Hartwich M., von Bergen M., Richnow H.H., Vogt C. (2008). Incorporation of carbon and nitrogen atoms into proteins measured by protein-based stable isotope probing (Protein-SIP)Rapid Commun Mass Spectrom 222889–2897 [View Article][PubMed]. [Google Scholar]
  25. Jones A.K., Lenz O., Strack A., Buhrke T., Friedrich B. (2004). NiFe hydrogenase active site biosynthesis: identification of Hyp protein complexes in Ralstonia eutropha Biochemistry 4313467–13477 [View Article][PubMed]. [Google Scholar]
  26. Kube M., Beck A., Zinder S.H., Kuhl H., Reinhardt R., Adrian L. (2005). Genome sequence of the chlorinated compound-respiring bacterium Dehalococcoides species strain CBDB1Nat Biotechnol 231269–1273 [View Article][PubMed]. [Google Scholar]
  27. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. (1951). Protein measurement with the Folin phenol reagentJ Biol Chem 193265–275[PubMed]. [Google Scholar]
  28. Lubitz W., Ogata H., Rüdiger O., Reijerse E. (2014). HydrogenasesChem Rev 1144081–4148 [View Article][PubMed]. [Google Scholar]
  29. Lutz S., Jacobi A., Schlensog V., Böhm R., Sawers G., Böck A. (1991). Molecular characterization of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli Mol Microbiol 5123–135 [View Article][PubMed]. [Google Scholar]
  30. Magalon A., Böck A. (2000). Analysis of the HypC-hycE complex, a key intermediate in the assembly of the metal center of the Escherichia coli hydrogenase 3J Biol Chem 27521114–21120 [View Article][PubMed]. [Google Scholar]
  31. Maier T., Jacobi A., Sauter M., Böck A. (1993). The product of the hypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding proteinJ Bacteriol 175630–635[PubMed]. [Google Scholar]
  32. Mansfeldt C.B., Rowe A.R., Heavner G.L., Zinder S.H., Richardson R.E. (2014). Meta-analyses of Dehalococcoides mccartyi strain 195 transcriptomic profiles identify a respiration rate-related gene expression transition point and interoperon recruitment of a key oxidoreductase subunitAppl Environ Microbiol 806062–6072 [View Article][PubMed]. [Google Scholar]
  33. Menon N.K., Chatelus C.Y., Dervartanian M., Wendt J.C., Shanmugam K.T., Peck H.D. Jr, Przybyla A.E. (1994). Cloning, sequencing, and mutational analysis of the hyb operon encoding Escherichia coli hydrogenase 2J Bacteriol 1764416–4423[PubMed]. [Google Scholar]
  34. Miller J.H. (1972). Experiments in molecular geneticsCold Spring Harbor, NYCold Spring Harbor Laboratory Press. [Google Scholar]
  35. Ogata H., Nishikawa K., Lubitz W. (2015). Hydrogens detected by subatomic resolution protein crystallography in a [NiFe] hydrogenaseNature 520571–574 [View Article][PubMed]. [Google Scholar]
  36. Paschos A., Bauer A., Zimmermann A., Zehelein E., Böck A. (2002). HypF, a carbamoyl phosphate-converting enzyme involved in [NiFe] hydrogenase maturationJ Biol Chem 27749945–49951 [View Article][PubMed]. [Google Scholar]
  37. Pinske C., Sawers R.G. (2014). The importance of iron in the biosynthesis and assembly of [NiFe]-hydrogenasesBiomol Concepts 555–70 [View Article][PubMed]. [Google Scholar]
  38. Pinske C., Krüger S., Soboh B., Ihling C., Kuhns M., Braussemann M., Jaroschinsky M., Sauer C., Sargent F., other authors. (2011). Efficient electron transfer from hydrogen to benzyl viologen by the [NiFe]-hydrogenases of Escherichia coli is dependent on the coexpression of the iron-sulfur cluster-containing small subunitArch Microbiol 193893–903 [View Article][PubMed]. [Google Scholar]
  39. Pinske C., Jaroschinsky M., Sargent F., Sawers G. (2012). Zymographic differentiation of [NiFe]-hydrogenases 1, 2 and 3 of Escherichia coli K-12BMC Microbiol 12134 [View Article][PubMed]. [Google Scholar]
  40. Pinske C., Jaroschinsky M., Linek S., Kelly C.L., Sargent F., Sawers R.G. (2015). Physiology and bioenergetics of [NiFe]-hydrogenase 2-catalyzed H2-consuming and H2-producing reactions in Escherichia coli J Bacteriol 197296–306 [View Article][PubMed]. [Google Scholar]
  41. Pöritz M., Goris T., Wubet T., Tarkka M.T., Buscot F., Nijenhuis I., Lechner U., Adrian L. (2013). Genome sequences of two dehalogenation specialists – Dehalococcoides mccartyi strains BTF08 and DCMB5 enriched from the highly polluted Bitterfeld regionFEMS Microbiol Lett 343101–104 [View Article][PubMed]. [Google Scholar]
  42. Redwood M.D., Mikheenko I.P., Sargent F., Macaskie L.E. (2008). Dissecting the roles of Escherichia coli hydrogenases in biohydrogen productionFEMS Microbiol Lett 27848–55 [View Article][PubMed]. [Google Scholar]
  43. Reissmann S., Hochleitner E., Wang H., Paschos A., Lottspeich F., Glass R.S., Böck A. (2003). Taming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligandsScience 2991067–1070 [View Article][PubMed]. [Google Scholar]
  44. Richard D.J., Sawers G., Sargent F., McWalter L., Boxer D.H. (1999). Transcriptional regulation in response to oxygen and nitrate of the operons encoding the [NiFe] hydrogenases 1 and 2 of Escherichia coli Microbiology 1452903–2912 [View Article][PubMed]. [Google Scholar]
  45. Sargent F., Ballantine S.P., Rugman P.A., Palmer T., Boxer D.H. (1998a). Reassignment of the gene encoding the Escherichia coli hydrogenase 2 small subunit–identification of a soluble precursor of the small subunit in a hypB mutantEur J Biochem 255746–754 [View Article][PubMed]. [Google Scholar]
  46. Sargent F., Bogsch E.G., Stanley N.R., Wexler M., Robinson C., Berks B.C., Palmer T. (1998b). Overlapping functions of components of a bacterial Sec-independent protein export pathwayEMBO J 173640–3650 [View Article][PubMed]. [Google Scholar]
  47. Sasaki D., Watanabe S., Matsumi R., Shoji T., Yasukochi A., Tagashira K., Fukuda W., Kanai T., Atomi H., other authors. (2013). Identification and structure of a novel archaeal HypB for [NiFe] hydrogenase maturationJ Mol Biol 4251627–1640 [View Article][PubMed]. [Google Scholar]
  48. Sawers R.G., Ballantine S.P., Boxer D.H. (1985). Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: evidence for a third isoenzymeJ Bacteriol 1641324–1331[PubMed]. [Google Scholar]
  49. Schiffels J., Selmer T. (2015) [View Article][PubMed] A flexible toolbox to study protein-assisted metalloenzyme assembly in vitro. Biotechnol Bioeng 1122360–2372. [Google Scholar]
  50. Schiffels J., Pinkenburg O., Schelden M., Aboulnaga H.A., Baumann M.E.M., Selmer T. (2013). An innovative cloning platform enables large-scale production and maturation of an oxygen-tolerant [NiFe]-hydrogenase from Cupriavidus necator in Escherichia coli PLoS One 8e68812 [View Article][PubMed]. [Google Scholar]
  51. Schlensog V., Böck A. (1990). Identification and sequence analysis of the gene encoding the transcriptional activator of the formate hydrogenlyase system of Escherichia coli Mol Microbiol 41319–1327 [View Article][PubMed]. [Google Scholar]
  52. Seshadri R., Adrian L., Fouts D.E., Eisen J.A., Phillippy A.M., Methe B.A., Ward N.L., Nelson W.C., Deboy R.T., other authors. (2005). Genome sequence of the PCE-dechlorinating bacterium Dehalococcoides ethenogenes Science 307105–108 [View Article][PubMed]. [Google Scholar]
  53. Soboh B., Pinske C., Kuhns M., Waclawek M., Ihling C., Trchounian K., Trchounian A., Sinz A., Sawers G. (2011). The respiratory molybdo-selenoprotein formate dehydrogenases of Escherichia coli have hydrogen: benzyl viologen oxidoreductase activityBMC Microbiol 11173 [View Article][PubMed]. [Google Scholar]
  54. Soboh B., Stripp S.T., Bielak C., Lindenstrauß U., Braussemann M., Javaid M., Hallensleben M., Granich C., Herzberg M., other authors. (2013). The [NiFe]-hydrogenase accessory chaperones HypC and HybG of Escherichia coli are iron- and carbon dioxide-binding proteinsFEBS Lett 5872512–2516 [View Article][PubMed]. [Google Scholar]
  55. Soboh B., Lindenstrauss U., Granich C., Javed M., Herzberg M., Thomas C., Stripp S.T. (2014). [NiFe]-hydrogenase maturation in vitro: analysis of the roles of the HybG and HypD accessory proteins1Biochem J 464169–177 [View Article][PubMed]. [Google Scholar]
  56. Stripp S.T., Soboh B., Lindenstrauss U., Braussemann M., Herzberg M., Nies D.H., Sawers R.G., Heberle J. (2013). HypD is the scaffold protein for Fe-(CN)2CO cofactor assembly in [NiFe]-hydrogenase maturationBiochemistry 523289–3296 [View Article][PubMed]. [Google Scholar]
  57. Sun J., Hopkins R.C., Jenney F.E. Jr, McTernan P.M., Adams M.W.W. (2010). Heterologous expression and maturation of an NADP-dependent [NiFe]-hydrogenase: a key enzyme in biofuel productionPLoS One 5e10526 [View Article][PubMed]. [Google Scholar]
  58. Vignais P.M., Billoud B. (2007). Occurrence, classification, and biological function of hydrogenases: an overviewChem Rev 1074206–4272 [View Article][PubMed]. [Google Scholar]
  59. Watanabe S., Matsumi R., Atomi H., Imanaka T., Miki K. (2012). Crystal structures of the HypCD complex and the HypCDE ternary complex: transient intermediate complexes during [NiFe] hydrogenase maturationStructure 202124–2137 [View Article][PubMed]. [Google Scholar]
  60. Watanabe S., Kawashima T., Nishitani Y., Kanai T., Wada T., Inaba K., Atomi H., Imanaka T., Miki K. (2015). Structural basis of a Ni acquisition cycle for [NiFe] hydrogenase by Ni-metallochaperone HypA and its enhancerProc Natl Acad Sci U S A 1127701–7706 [View Article][PubMed]. [Google Scholar]
  61. Waugh R., Boxer D.H. (1986). Pleiotropic hydrogenase mutants of Escherichia coli K12: growth in the presence of nickel can restore hydrogenase activityBiochimie 68157–166 [View Article][PubMed]. [Google Scholar]
  62. Weyman P.D., Vargas W.A., Chuang R.Y., Chang Y., Smith H.O., Xu Q. (2011). Heterologous expression of Alteromonas macleodii and Thiocapsa roseopersicina [NiFe] hydrogenases in Escherichia coli Microbiology 1571363–1374 [View Article][PubMed]. [Google Scholar]
  63. Winter G., Buhrke T., Lenz O., Jones A.K., Forgber M., Friedrich B. (2005). A model system for [NiFe] hydrogenase maturation studies: Purification of an active site-containing hydrogenase large subunit without small subunitFEBS Lett 5794292–4296 [View Article][PubMed]. [Google Scholar]
  64. Wolf I., Buhrke T., Dernedde J., Pohlmann A., Friedrich B. (1998). Duplication of hyp genes involved in maturation of [NiFe] hydrogenases in Alcaligenes eutrophus H16Arch Microbiol 170451–459 [View Article][PubMed]. [Google Scholar]
  65. Yonemoto I.T., Smith H.O., Weyman P.D. (2015). Designed surface residue substitutions in [NiFe] hydrogenase that improve electron transfer characteristicsInt J Mol Sci 162020–2033 [View Article][PubMed]. [Google Scholar]
  66. Zhang J.W., Butland G., Greenblatt J.F., Emili A., Zamble D.B. (2005). A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathwayJ Biol Chem 2804360–4366 [View Article][PubMed]. [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000177
Loading
Heterologous complementation studies in Escherichia coli with the Hyp accessory protein machinery from Chloroflexi provide insight into [NiFe]-hydrogenase large subunit recognition by the HypC protein family
Microbiology 161, 2204 (2015); https://doi.org/10.1099/mic.0.000177
/content/journal/micro/10.1099/mic.0.000177
/content/journal/micro/10.1099/mic.0.000177
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error