1887

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 .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032771-0
2010-06-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/6/1575.html?itemId=/content/journal/micro/10.1099/mic.0.032771-0&mimeType=html&fmt=ahah

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.[CrossRef]
    [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.[CrossRef]
    [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 [CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  12. Hedderich, R. & Forzi, L. ( 2005; ). Energy-converting [NiFe] hydrogenases: more than just H2 activation. J Mol Microbiol Biotechnol 10, 92–104.[CrossRef]
    [Google Scholar]
  13. Heinekey, D. M. ( 2009; ). Hydrogenase enzymes: recent studies and active site models. J Organomet Chem 694, 2671–2680.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  16. Katoh, K. & Toh, H. ( 2008; ). Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9, 286–298.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  30. Mathews, J. & Wang, G. ( 2009; ). Metabolic pathway engineering for enhanced biohydrogen production. Int J Hydrogen Energy 34, 7404–7416.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  33. Meyer, J. ( 2007; ). [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64, 1063–1084.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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 1757, 1582–1591.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [Google Scholar]
  59. Woodward, J., Orr, M., Cordray, K. & Greenbaum, E. ( 2000; ). Enzymatic production of biohydrogen. Nature 405, 1014–1015.[CrossRef]
    [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.[CrossRef]
    [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.[CrossRef]
    [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 [CrossRef]
    [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.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032771-0
Loading
/content/journal/micro/10.1099/mic.0.032771-0
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