1887

Abstract

The membrane-associated formate hydrogenlyase (FHL) complex of bacteria like is responsible for the disproportionation of formic acid into the gaseous products carbon dioxide and dihydrogen. It comprises minimally seven proteins including FdhF and HycE, the catalytic subunits of formate dehydrogenase H and hydrogenase 3, respectively. Four proteins of the FHL complex have iron–sulphur cluster ([Fe–S]) cofactors. Biosynthesis of [Fe–S] is principally catalysed by the Isc or Suf systems and each comprises proteins for assembly and for delivery of [Fe–S]. This study demonstrates that the Isc system is essential for biosynthesis of an active FHL complex. In the absence of the IscU assembly protein no hydrogen production or activity of FHL subcomponents was detected. A deletion of the gene also resulted in reduced intracellular formate levels partially due to impaired synthesis of pyruvate formate-lyase, which is dependent on the [Fe–S]-containing regulator FNR. This caused reduced expression of the formate-inducible gene. The A-type carrier (ATC) proteins IscA and ErpA probably deliver [Fe–S] to specific apoprotein components of the FHL complex because mutants lacking either protein exhibited strongly reduced hydrogen production. Neither ATC protein could compensate for the lack of the other, suggesting that they had independent roles in [Fe–S] delivery to complex components. Together, the data indicate that the Isc system modulates FHL complex biosynthesis directly by provision of [Fe–S] as well as indirectly by influencing gene expression through the delivery of [Fe–S] to key regulators and enzymes that ultimately control the generation and oxidation of formate.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.066142-0
2013-06-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/6/1179.html?itemId=/content/journal/micro/10.1099/mic.0.066142-0&mimeType=html&fmt=ahah

References

  1. Axley M. J. , Grahame D. A. , Stadtman T. C. . ( 1990; ). Escherichia coli formate-hydrogen lyase. Purification and properties of the selenium-dependent formate dehydrogenase component. . J Biol Chem 265:, 18213–18218.[PubMed]
    [Google Scholar]
  2. Ayala-Castro C. , Saini A. , Outten F. W. . ( 2008; ). Fe-S cluster assembly pathways in bacteria. . Microbiol Mol Biol Rev 72:, 110–125. [CrossRef] [PubMed]
    [Google Scholar]
  3. 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 collection. . Mol Syst Biol 2:, 2006.0008.[CrossRef]
    [Google Scholar]
  4. Ballantine S. P. , Boxer D. H. . ( 1985; ). Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12. . J Bacteriol 163:, 454–459.[PubMed]
    [Google Scholar]
  5. Begg Y. A. , Whyte J. N. , Haddock B. A. . ( 1977; ). The identification of mutants of Escherichia coli deficient in formate dehydrogenase and nitrate reductase activities using dye indicator plates. . FEMS Microbiol Lett 2:, 47–50. [CrossRef]
    [Google Scholar]
  6. Beyer L. , Doberenz C. , Falke D. , Hunger D. , Suppmann B. , Sawers R. G. . ( 2013; ). Coordination of FocA and pyruvate formate-lyase synthesis in Escherichia coli demonstrates preferential translocation of formate over other mixed-acid fermentation products. . J Bacteriol 195:, 1428–1435. [CrossRef] [PubMed]
    [Google Scholar]
  7. Birkmann A. , Zinoni F. , Sawers G. , Böck A. . ( 1987; ). Factors affecting transcriptional regulation of the formate-hydrogen-lyase pathway of Escherichia coli . . Arch Microbiol 148:, 44–51. [CrossRef] [PubMed]
    [Google Scholar]
  8. 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]-hydrogenases. . J Mol Biol 344:, 155–167. [CrossRef] [PubMed]
    [Google Scholar]
  9. Böck A. , King P. W. , Blokesch M. , Posewitz M. C. . ( 2006; ). Maturation of hydrogenases. . Adv Microb Physiol 51:, 1–71. [CrossRef] [PubMed]
    [Google Scholar]
  10. Böhm R. , Sauter M. , Böck A. . ( 1990; ). Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. . Mol Microbiol 4:, 231–243. [CrossRef] [PubMed]
    [Google Scholar]
  11. Boyington J. C. , Gladyshev V. N. , Khangulov S. V. , Stadtman T. C. , Sun P. D. . ( 1997; ). Crystal structure of formate dehydrogenase H: catalysis involving Mo, molybdopterin, selenocysteine, and an Fe4S4 cluster. . Science 275:, 1305–1308. [CrossRef] [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 Mu. . J Mol Biol 104:, 541–555. [CrossRef] [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 determinant. . Gene 158:, 9–14. [CrossRef] [PubMed]
    [Google Scholar]
  14. Eitinger T. , Mandrand-Berthelot M. A. . ( 2000; ). Nickel transport systems in microorganisms. . Arch Microbiol 173:, 1–9. [CrossRef] [PubMed]
    [Google Scholar]
  15. Falke D. , Schulz K. , Doberenz C. , Beyer L. , Lilie H. , Thiemer B. , Sawers R. G. . ( 2010; ). Unexpected oligomeric structure of the FocA formate channel of Escherichia coli : a paradigm for the formate–nitrite transporter family of integral membrane proteins. . FEMS Microbiol Lett 303:, 69–75. [CrossRef] [PubMed]
    [Google Scholar]
  16. Forzi L. , Sawers R. G. . ( 2007; ). Maturation of [NiFe]-hydrogenases in Escherichia coli. . Biometals 20:, 565–578. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hesslinger C. , Fairhurst S. A. , Sawers G. . ( 1998; ). Novel keto acid formate-lyase and propionate kinase enzymes are components of an anaerobic pathway in Escherichia coli that degrades L-threonine to propionate. . Mol Microbiol 27:, 477–492. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hormann K. , Andreesen J. . ( 1989; ). Reductive cleavage of sarcosine and betaine by Eubacterium acidaminophilum via enzyme systems different from glycine reductase. . Arch Microbiol 153:, 50–59. [CrossRef]
    [Google Scholar]
  19. Johnson D. C. , Dean D. R. , Smith A. D. , Johnson M. K. . ( 2005; ). Structure, function, and formation of biological iron-sulfur clusters. . Annu Rev Biochem 74:, 247–281. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kim Y. J. , Lee H. S. , Kim E. S. , Bae S. S. , Lim J. K. , Matsumi R. , Lebedinsky A. V. , Sokolova T. G. , Kozhevnikova D. A. . & other authors ( 2010; ). Formate-driven growth coupled with H2 production. . Nature 467:, 352–355. [CrossRef] [PubMed]
    [Google Scholar]
  21. Knappe J. , Sawers G. . ( 1990; ). A radical-chemical route to acetyl-CoA: the anaerobically induced pyruvate formate-lyase system of Escherichia coli. . FEMS Microbiol Rev 6:, 383–398. [CrossRef] [PubMed]
    [Google Scholar]
  22. Laemmli U. K. . ( 1970; ). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. . Nature 227:, 680–685. [CrossRef] [PubMed]
    [Google Scholar]
  23. Loiseau L. , Gerez C. , Bekker M. , Ollagnier-de Choudens S. , Py B. , Sanakis Y. , Teixeira de Mattos J. , Fontecave M. , Barras F. . ( 2007; ). ErpA, an iron-sulfur (Fe–S) protein of the A-type essential for respiratory metabolism in Escherichia coli. . Proc Natl Acad Sci U S A 104:, 13626–13631. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lowry O. H. , Rosebrough N. J. , Farr A. L. , Randall R. J. . ( 1951; ). Protein measurement with the Folin phenol reagent. . J Biol Chem 193:, 265–275.[PubMed]
    [Google Scholar]
  25. Magalon A. , Böck A. . ( 2000; ). Dissection of the maturation reactions of the [NiFe] hydrogenase 3 from Escherichia coli taking place after nickel incorporation. . FEBS Lett 473:, 254–258. [CrossRef] [PubMed]
    [Google Scholar]
  26. Mettert E. L. , Outten F. W. , Wanta B. , Kiley P. J. . ( 2008; ). The impact of O2 on the Fe–S cluster biogenesis requirements of Escherichia coli FNR. . J Mol Biol 384:, 798–811. [CrossRef] [PubMed]
    [Google Scholar]
  27. Miller J. . ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor:: Cold Spring Harbor Laboratory Press;.
    [Google Scholar]
  28. Nakamura M. , Saeki K. , Takahashi Y. . ( 1999; ). Hyperproduction of recombinant ferredoxins in Escherichia coli by coexpression of the ORF1-ORF2-iscS-iscU-iscA-hscB-hscA-fdx-ORF3 gene cluster. . J Biochem 126:, 10–18. [CrossRef] [PubMed]
    [Google Scholar]
  29. Paschos A. , Bauer A. , Zimmermann A. , Zehelein E. , Böck A. . ( 2002; ). HypF, a carbamoyl phosphate-converting enzyme involved in [NiFe] hydrogenase maturation. . J Biol Chem 277:, 49945–49951. [CrossRef] [PubMed]
    [Google Scholar]
  30. Pinske C. , Sawers R. G. . ( 2010; ). The role of the ferric-uptake regulator Fur and iron homeostasis in controlling levels of the [NiFe]-hydrogenases in Escherichia coli. . Int J Hydrogen Energy 35:, 8938–8944. [CrossRef]
    [Google Scholar]
  31. Pinske C. , Sawers R. G. . ( 2012a; ). Delivery of iron-sulfur clusters to the hydrogen-oxidizing [NiFe]-hydrogenases in Escherichia coli requires the A-type carrier proteins ErpA and IscA. . PLoS ONE 7:, e31755. [CrossRef] [PubMed]
    [Google Scholar]
  32. Pinske C. , Sawers R. G. . ( 2012b; ). A-type carrier protein ErpA is essential for formation of an active formate-nitrate respiratory pathway in Escherichia coli K-12. . J Bacteriol 194:, 346–353. [CrossRef] [PubMed]
    [Google Scholar]
  33. Pinske C. , Bönn M. , Krüger S. , Lindenstrauss U. , Sawers R. G. . ( 2011; ). Metabolic deficiencies revealed in the biotechnologically important model bacterium Escherichia coli BL21(DE3). . PLoS ONE 6:, e22830. [CrossRef] [PubMed]
    [Google Scholar]
  34. 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. [CrossRef] [PubMed]
    [Google Scholar]
  35. Py B. , Barras F. . ( 2010; ). Building Fe-S proteins: bacterial strategies. . Nat Rev Microbiol 8:, 436–446. [CrossRef] [PubMed]
    [Google Scholar]
  36. Py B. , Gerez C. , Angelini S. , Planel R. , Vinella D. , Loiseau L. , Talla E. , Brochier-Armanet C. , Garcia Serres R. . & other authors ( 2012; ). Molecular organization, biochemical function, cellular role and evolution of NfuA, an atypical Fe-S carrier. . Mol Microbiol 86:, 155–171. [CrossRef] [PubMed]
    [Google Scholar]
  37. Rossmann R. , Sawers G. , Böck A. . ( 1991; ). Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. . Mol Microbiol 5:, 2807–2814. [CrossRef] [PubMed]
    [Google Scholar]
  38. Sauter M. , Sawers R. G. . ( 1990; ). Transcriptional analysis of the gene encoding pyruvate formate-lyase-activating enzyme of Escherichia coli. . Mol Microbiol 4:, 355–363. [CrossRef] [PubMed]
    [Google Scholar]
  39. Sauter M. , Böhm R. , Böck A. . ( 1992; ). Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. . Mol Microbiol 6:, 1523–1532. [CrossRef] [PubMed]
    [Google Scholar]
  40. Sawers G. , Böck A. . ( 1988; ). Anaerobic regulation of pyruvate formate-lyase from Escherichia coli K-12. . J Bacteriol 170:, 5330–5336.[PubMed]
    [Google Scholar]
  41. Sawers G. , Suppmann B. . ( 1992; ). Anaerobic induction of pyruvate formate-lyase gene expression is mediated by the ArcA and FNR proteins. . J Bacteriol 174:, 3474–3478.[PubMed]
    [Google Scholar]
  42. Sawers R. G. , Ballantine S. P. , Boxer D. H. . ( 1985; ). Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: evidence for a third isoenzyme. . J Bacteriol 164:, 1324–1331.[PubMed]
    [Google Scholar]
  43. Sawers R. G. , Blokesch M. , Böck A. . ( 2004; ). Anaerobic formate and hydrogen metabolism. September 2004, posting date. . Chapter 3.5.4. In EcoSal – Escherichia coli and Salmonella: Cellular and Molecular Biology. Edited by Curtiss R. III . and others. American Society for Microbiology;, Washington, DC:. http://www.ecosal.org.
    [Google Scholar]
  44. Simons R. W. , Houman F. , Kleckner N. . ( 1987; ). Improved single and multicopy lac-based cloning vectors for protein and operon fusions. . Gene 53:, 85–96. [CrossRef] [PubMed]
    [Google Scholar]
  45. 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 activity. . BMC Microbiol 11:, 173. [CrossRef] [PubMed]
    [Google Scholar]
  46. Suppmann B. , Sawers G. . ( 1994; ). Isolation and characterization of hypophosphite-resistant mutants of Escherichia coli: identification of the FocA protein, encoded by the pfl operon, as a putative formate transporter. . Mol Microbiol 11:, 965–982. [CrossRef] [PubMed]
    [Google Scholar]
  47. Takahashi Y. , Tokumoto U. . ( 2002; ). A third bacterial system for the assembly of iron-sulfur clusters with homologs in archaea and plastids. . J Biol Chem 277:, 28380–28383. [CrossRef] [PubMed]
    [Google Scholar]
  48. Towbin H. , Staehelin T. , Gordon J. . ( 1979; ). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. . Proc Natl Acad Sci U S A 76:, 4350–4354. [CrossRef] [PubMed]
    [Google Scholar]
  49. Vinella D. , Brochier-Armanet C. , Loiseau L. , Talla E. , Barras F. . ( 2009; ). Iron-sulfur (Fe/S) protein biogenesis: phylogenomic and genetic studies of A-type carriers. . PLoS Genet 5:, e1000497. [CrossRef] [PubMed]
    [Google Scholar]
  50. Watanabe S. , Matsumi R. , Arai T. , Atomi H. , Imanaka T. , Miki K. . ( 2007; ). Crystal structures of [NiFe] hydrogenase maturation proteins HypC, HypD, and HypE: insights into cyanation reaction by thiol redox signaling. . Mol Cell 27:, 29–40. [CrossRef] [PubMed]
    [Google Scholar]
  51. Zinoni F. , Birkmann A. , Stadtman T. C. , Böck A. . ( 1986; ). Nucleotide sequence and expression of the selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. . Proc Natl Acad Sci U S A 83:, 4650–4654. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.066142-0
Loading
/content/journal/micro/10.1099/mic.0.066142-0
Loading

Data & Media loading...

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