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Volume 156, Issue 6

The surprising diversity of clostridial hydrogenases: a comparative genomic perspective Free

Abstract

Among the large variety of micro-organisms capable of fermentative hydrogen production, strict anaerobes such as members of the genus are the most widely studied. They can produce hydrogen by a reversible reduction of protons accumulated during fermentation to dihydrogen, a reaction which is catalysed by hydrogenases. Sequenced genomes provide completely new insights into the diversity of clostridial hydrogenases. Building on previous reports, we found that [FeFe] hydrogenases are not a homogeneous group of enzymes, but exist in multiple forms with different modular structures and are especially abundant in members of the genus . This unusual diversity seems to support the central role of hydrogenases in cell metabolism. In particular, the presence of multiple putative operons encoding multisubunit [FeFe] hydrogenases highlights the fact that hydrogen metabolism is very complex in this genus. In contrast with [FeFe] hydrogenases, their [NiFe] hydrogenase counterparts, widely represented in other bacteria and archaea, are found in only a few clostridial species. Surprisingly, a heteromultimeric Ech hydrogenase, known to be an energy-converting [NiFe] hydrogenase and previously described only in methanogenic archaea and some sulfur-reducing bacteria, was found to be encoded by the genomes of four cellulolytic strains: , , and .

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Keyword(s): Ech, energy-converting hydrogenases , FDH, formate dehydrogenase-like protein , FeS, iron–sulfur and RRR, rubrerythrin
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2010-06-01
2024-04-20
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References

  1. Balk J., Pierik A. J., Netz D. J., Mühlenhoff U., Lill R. 2004; The hydrogenase-like Nar1p is essential for maturation of cytosolic and nuclear iron-sulphur proteins. EMBO J 23:2105–2115
     [Google Scholar]
  2. Bartacek J., Zabranska J., Lens P. N. L. 2007; Developments and constraints in fermentative hydrogen production. Biofuels Bioprod Bioref 1:201–214
     [Google Scholar]
  3. Böck A., King P. W., Blokesch M., Posewitz M. C. 2006; Maturation of hydrogenases. Adv Microb Physiol 51:1–71
     [Google Scholar]
  4. Burroughs A. M., Balaji S., Iyer L. M., Aravind L. 2007; Small but versatile: the extraordinary functional and structural diversity of the β-grasp fold. Biol Direct 2:18
     [Google Scholar]
  5. Demuez M., Cournac L., Guerrini O., Soucaille P., Girbal L. 2007; Complete activity profile of Clostridium acetobutylicum [FeFe]-hydrogenase and kinetic parameters for endogenous redox partners. FEMS Microbiol Lett 275:113–121
     [Google Scholar]
  6. Dubini A., Sargent F. 2003; Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Lett 549:141–146
     [Google Scholar]
  7. Fang H. H., Liu H. 2002; Effect of pH on hydrogen production from glucose by a mixed culture. Bioresour Technol 82:87–93
     [Google Scholar]
  8. Friedrich B., Buhrke T., Burgdorf T., Lenz O. 2005; A hydrogen-sensing multiprotein complex controls aerobic hydrogen metabolism in Ralstonia eutropha. Biochem Soc Trans 33:97–101
     [Google Scholar]
  9. Gardy J. L., Laird M. R., Chen F., Rey S., Walsh C. J., Ester M., Brinkman F. S. L. 2005; PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 21:617–623
     [Google Scholar]
  10. Graentzdoerffer A., Rauh D., Pich A., Andreesen J. R. 2003; Molecular and biochemical characterization of two tungsten- and selenium-containing formate dehydrogenases from Eubacterium acidaminophilum that are associated with components of an iron-only hydrogenase. Arch Microbiol 179:116–130
     [Google Scholar]
  11. Hallenbeck P. C., Benemann J. R. 2002; Biological hydrogen production; fundamentals and limiting processes. Int J Hydrogen Energy 27:1185–1193
     [Google Scholar]
  12. Hedderich R., Forzi L. 2005; Energy-converting [NiFe] hydrogenases: more than just H2 activation. J Mol Microbiol Biotechnol 10:92–104
     [Google Scholar]
  13. Heinekey D. M. 2009; Hydrogenase enzymes: recent studies and active site models. J Organomet Chem 694:2671–2680
     [Google Scholar]
  14. Herrmann G., Jayamani E., Mai G., Buckel W. 2008; Energy conservation via electron-transferring flavoprotein in anaerobic bacteria. J Bacteriol 190:784–791
     [Google Scholar]
  15. Kaji M., Taniguchi Y., Matsushita O., Katayama S., Miyata S., Morita S., Okabe A. 1999; The hydA gene encoding the H2-evolving hydrogenase of Clostridium perfringens: molecular characterization and expression of the gene. FEMS Microbiol Lett 181:329–336
     [Google Scholar]
  16. Katoh K., Toh H. 2008; Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298
     [Google Scholar]
  17. Khanal S. K., Chen W.-H., Li L., Sung S. 2004; Biological hydrogen production: effects of pH and intermediate products. Int J Hydrogen Energy 29:1123–1131
     [Google Scholar]
  18. 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
     [Google Scholar]
  19. Kurkin S., Meuer J., Koch J., Hedderich R., Albracht S. P. J. 2002; The membrane-bound [NiFe]-hydrogenase (Ech) from Methanosarcina barkeri: unusual properties of the iron-sulphur clusters. Eur J Biochem 269:6101–6111
     [Google Scholar]
  20. Levin D. B., Pitt L., Love M. 2004; Biohydrogen production: prospects and limitations to practical application. Int J Hydrogen Energy 29:173–185
     [Google Scholar]
  21. Li C., Fang H. H. P. 2007; Fermentative hydrogen production from wastewater and solid wastes by mixed cultures. Crit Rev Environ Sci Technol 37:1–39
     [Google Scholar]
  22. Li M., Liu M. Y., LeGall J., Gui L. L., Liao J., Jiang T., Zhang J. P., Liang D. C., Chang W. R. 2003; Crystal structure studies on rubrerythrin: enzymatic activity in relation to the zinc movement. J Biol Inorg Chem 8:149–155
     [Google Scholar]
  23. Lin P. Y., Whang L. M., Wu Y. R., Ren W. J., Hsiao C. J., Li S. L., Chang J. S. 2007; Biological hydrogen production of the genus Clostridium: metabolic study and mathematical model simulation. Int J Hydrogen Energy 32:1728–1735
     [Google Scholar]
  24. Liu X., Zhu Y., Yang S. T. 2005; Butyric acid and hydrogen production by Clostridium tyrobutyricum ATCC 25755 and mutants. Enzyme Microb Technol 38:521–528
     [Google Scholar]
  25. Liu Y., Yu P., Song X., Qu Y. 2008; Hydrogen production from cellulose by co-culture of Clostridium thermocellum JN4 and Thermoanaerobacterium thermosaccharolyticum GD17. Int J Hydrogen Energy 33:2927–2933
     [Google Scholar]
  26. Maeda T., Sanchez-Torres V., Wood T. K. 2007; Escherichia coli hydrogenase 3 is a reversible enzyme possessing hydrogen uptake and synthesis activities. Appl Microbiol Biotechnol 76:1035–1042
     [Google Scholar]
  27. Marchler-Bauer A., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C., Gonzales N. R. other authors 2009; CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37:D205–D210
     [Google Scholar]
  28. Masepohl B., Kutsche M., Riedel K. U., Schmehl M., Klipp W., Pühler A. 1992; Functional analysis of the cysteine motifs in the ferredoxin-like protein FdxN of Rhizobium meliloti involved in symbiotic nitrogen fixation. Mol Gen Genet 233:33–41
     [Google Scholar]
  29. Masukawa H., Mochimaru M., Sakura H. 2002; Hydrogenases and photobiological hydrogen production utilizing nitrogenase system in cyanobacteria. Int J Hydrogen Energy 27:1471–1474
     [Google Scholar]
  30. Mathews J., Wang G. 2009; Metabolic pathway engineering for enhanced biohydrogen production. Int J Hydrogen Energy 34:7404–7416
     [Google Scholar]
  31. Meek L., Arp D. J. 2000; The hydrogenase cytochrome b heme ligands of Azotobacter vinelandii are required for full H2 oxidation capability. J Bacteriol 182:3429–3436
     [Google Scholar]
  32. Meuer J., Kuettner H. C., Zhang J. K., Hedderich R., Metcalf W. 2002; Genetic analysis of the archaeon Methanosarcina barkeri Fusaro reveals a central role for Ech hydrogenase and ferredoxin in methanogenesis and carbon fixation. Proc Natl Acad Sci U S A 99:5632–5637
     [Google Scholar]
  33. Meyer J. 2007; [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64:1063–1084
     [Google Scholar]
  34. Morimoto K., Kimura T., Sakka K., Ohmiya K. 2005; Overexpression of a hydrogenase gene in Clostridium paraputrificum to enhance hydrogen gas production. FEMS Microbiol Lett 246:229–234
     [Google Scholar]
  35. Nath K., Das D. 2004; Improvement for fermentative hydrogen production: various approaches. Appl Microbiol Biotechnol 65:520–529
     [Google Scholar]
  36. Nicolet Y., Piras C., Legrand P., Hatchikian C. E., Fontecilla-Camps J. C. 1999; Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7:13–23
     [Google Scholar]
  37. Nicolet Y., Lemon B. J., Fontecilla-Camps J. C., Peters J. W. 2000; A novel FeS cluster in Fe-only hydrogenases. Trends Biochem Sci 25:138–143
     [Google Scholar]
  38. Pereira P. M., He Q., Valente F. M. A., Xavier A. V., Zhou J., Pereira I. A. C., Louro L. O. 2008; Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis. Antonie van Leeuwenhoek 93:347–362
     [Google Scholar]
  39. Peters J. W., Lanzilotta W. N., Lemon B. J., Seefeldt L. C. 1998; X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 Angstrom resolution. Science 282:1853–1858
     [Google Scholar]
  40. Pierik A. J., Wolbert R. B., Portier G. L., Verhagen M. F., Hagen W. R. 1993; Nigerythrin and rubrerythrin from Desulfovibrio vulgaris each contain two mononuclear iron centers and two dinuclear iron clusters. Eur J Biochem 212:237–245
     [Google Scholar]
  41. Pilak O., Mamat B., Vogt S., Hagemeier C. H., Thauer R. K., Shima S., Vonrhein C., Warkentin E., Ermler U. 2006; The crystal structure of the apoenzyme of the iron-sulfur cluster-free hydrogenase. J Mol Biol 358:798–809
     [Google Scholar]
  42. Posewitz M. C., King P. W., Smolinski S. L., Zhang L., Seibert M., Ghirardi M. L. 2004; Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711–25720
     [Google Scholar]
  43. Rodrigues R., Valente F. M. A., Pereira I. A. C., Oliveira S., Rodrigues-Pousada C. 2003; A novel membrane-bound Ech [NiFe] hydrogenase in Desulfovibrio gigas. Biochem Biophys Res Commun 306:366–375
     [Google Scholar]
  44. Sadana J. C., Rittenberg D. 1963; Some observations on the enzyme hydrogenase of Desulfovibrio desulfuricans. Proc Natl Acad Sci U S A 50:900–904
     [Google Scholar]
  45. Schut G. J., Adams M. W. 2009; The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191:4451–4457
     [Google Scholar]
  46. Self W. T., Hasona A., Shanmugam K. T. 2004; Expression and regulation of a silent operon, hyf, coding for hydrogenase 4 isoenzyme in Escherichia coli. J Bacteriol 186:580–587
     [Google Scholar]
  47. Singer S. W., Hirst M. B., Ludden P. W. 2006; CO-dependent H2 evolution by Rhodospirillum rubrum: role of CODH : CooF complex. Biochim Biophys Acta 17571582–1591
     [Google Scholar]
  48. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599
     [Google Scholar]
  49. Van Ginkel S. W., Oh S. E., Logan B. E. 2005; Biohydrogen gas production from food processing and domestic wastewaters. Int J Hydrogen Energy 30:1535–1542
     [Google Scholar]
  50. Vanoni M. A., Curti B. 2008; Structure–function studies of glutamate synthases: a class of self-regulated iron-sulfur flavoenzymes essential for nitrogen assimilation. IUBMB Life 60:287–300
     [Google Scholar]
  51. Vardar-Schara G., Maeda T., Wood T. K. 2007; Metabolically engineered bacteria for producing hydrogen via fermentation. Microbiol Biotechnol 1:107–125
     [Google Scholar]
  52. Verhagen M. F., O'Rourke T., Adams M. W. 1999; The hyperthermophilic bacterium, Thermotoga maritima, contains an unusually complex iron-hydrogenase: amino acid sequence analyses versus biochemical characterization. Biochim Biophys Acta 1412:212–229
     [Google Scholar]
  53. Vignais P. M. 2008; Hydrogenases and H+-reduction in primary energy conservation. Results Probl Cell Differ 45:223–252
     [Google Scholar]
  54. Vignais P. M., Colbeau A. 2004; Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188
     [Google Scholar]
  55. Vignais P. M., Billoud B., Meyer J. 2001; Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501
     [Google Scholar]
  56. Volbeda A., Charon M. H., Piras C., Hatchikian E. C., Frey M., Fontecilla-Camps J. C. 1995; Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373:580–587
     [Google Scholar]
  57. Wang M. Y., Tsai Y. L., Olson B. H., Chang J. S. 2008a; Monitoring dark hydrogen fermentation performance of indigenous Clostridium butyricum by hydrogenase gene expression using RT-PCR and qPCR. Int J Hydrogen Energy 33:4730–4738
     [Google Scholar]
  58. Wang M. Y., Olson B. H., Chang J. S. 2008b; Relationship among growth parameters for Clostridium butyricum, hydA gene expression, and biohydrogen production in a sucrose-supplemented batch reactor. Appl Microbiol Biotechnol 78:525–532
     [Google Scholar]
  59. Woodward J., Orr M., Cordray K., Greenbaum E. 2000; Enzymatic production of biohydrogen. Nature 405:1014–1015
     [Google Scholar]
  60. Wu L. F., Ize B., Chanal A., Quentin Y., Fichant G. 2000; Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J Mol Microbiol Biotechnol 2:179–189
     [Google Scholar]
  61. Yang K., Metcalf W. W. 2004; A new activity for an old enzyme: Escherichia coli bacterial alkaline phosphatase is a phosphite-dependent hydrogenase. Proc Natl Acad Sci U S A 101:7919–7924
     [Google Scholar]
  62. Yates M. G., De Souza E. M., Kahindi J. H. 1997; Oxygen, hydrogen and nitrogen fixation in Azotobacter. Soil Biol Biochem 29:863–869
     [Google Scholar]
  63. Zhang Y. H. P., Evans B. R., Mielenz J. R., Hopkins R. C., Adams M. W. W. 2007; High-yield hydrogen production from starch and water by a synthetic enzymatic pathway. PLoS One 2:e456
     [Google Scholar]
  64. Zhulin I. B., Taylor B. L., Dixon R. 1997; PAS domain S-boxes in archaea, bacteria and sensors for oxygen and redox. Trends Biochem Sci 22:331–333
     [Google Scholar]
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The surprising diversity of clostridial hydrogenases: a comparative genomic perspective
Microbiology 156, 1575 (2010); https://doi.org/10.1099/mic.0.032771-0
/content/journal/micro/10.1099/mic.0.032771-0
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