Advertisement

Clostridial whole cell and enzyme systems for hydrogen production: current state and perspectives

  • Amel Latifi
  • Luisana Avilan
  • Myriam Brugna
Mini-Review

Abstract

Strictly anaerobic bacteria of the Clostridium genus have attracted great interest as potential cell factories for molecular hydrogen production purposes. In addition to being a useful approach to this process, dark fermentation has the advantage of using the degradation of cheap agricultural residues and industrial wastes for molecular hydrogen production. However, many improvements are still required before large-scale hydrogen production from clostridial metabolism is possible. Here we review the literature on the basic biological processes involved in clostridial hydrogen production, and present the main advances obtained so far in order to enhance the hydrogen productivity, as well as suggesting some possible future prospects.

Keywords

Clostridia Fermentation Hydrogen production Hydrogenase Metabolic engineering 

Notes

Funding

This study was funded by the “Agence Nationale pour la Recherche Scientifique” (ANR-13-BIME-0001).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Adams MW (1990) The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1020(2):115–145CrossRefGoogle Scholar
  2. Akhtar MK, Jones PR (2009) Construction of a synthetic YdbK-dependent pyruvate:H2 pathway in Escherichia coli BL21(DE3). Metab Eng 11(3):139–147.  https://doi.org/10.1016/j.ymben.2009.01.002 CrossRefPubMedGoogle Scholar
  3. Artz JH, Mulder DW, Ratzloff MW, Lubner CE, Zadvornyy OA, LeVan AX, Williams SG, Adams MWW, Jones AK, King PW, Peters JW (2017) Reduction potentials of [FeFe]-hydrogenase accessory iron-sulfur clusters provide insights into the energetics of proton reduction catalysis. J Am Chem Soc 139(28):9544–9550.  https://doi.org/10.1021/jacs.7b02099 CrossRefPubMedGoogle Scholar
  4. Avilan L, Roumezi B, Risoul V, Bernard CS, Kpebe A, Belhadjhassine M, Rousset M, Brugna M, Latifi A (2018) Phototrophic hydrogen production from a clostridial [FeFe] hydrogenase expressed in the heterocysts of the cyanobacterium Nostoc PCC 7120. Appl Microbiol Biotechnol 102(13):5775–5783.  https://doi.org/10.1007/s00253-018-8989-2 CrossRefPubMedGoogle Scholar
  5. Banu JR, Kannah RY, Kumar MD, Gunasekaran M, Sivagurunathan P, Park JH, Kumar G (2018) Recent advances on biogranules formation in dark hydrogen fermentation system: mechanism of formation and microbial characteristics. Bioresour Technol 268:787–796.  https://doi.org/10.1016/j.biortech.2018.07.034 CrossRefPubMedGoogle Scholar
  6. Bayer EA, Belaich JP, Shoham Y, Lamed R (2004) The cellulosomes: multienzyme machines for degradation of plant cell wall polysaccharides. Annu Rev Microbiol 58:521–554.  https://doi.org/10.1146/annurev.micro.57.030502.091022 CrossRefPubMedGoogle Scholar
  7. Benomar S, Ranava D, Cardenas ML, Trably E, Rafrafi Y, Ducret A, Hamelin J, Lojou E, Steyer JP, Giudici-Orticoni MT (2015) Nutritional stress induces exchange of cell material and energetic coupling between bacterial species. Nat Commun 6:6283.  https://doi.org/10.1038/ncomms7283 CrossRefPubMedGoogle Scholar
  8. Broderick JB, Byer AS, Duschene KS, Duffus BR, Betz JN, Shepard EM, Peters JW (2014) H-cluster assembly during maturation of the [FeFe]-hydrogenase. J Biol Inorg Chem 19(6):747–757.  https://doi.org/10.1007/s00775-014-1168-8 CrossRefPubMedGoogle Scholar
  9. Buckel W, Thauer RK (2013) Energy conservation via electron bifurcating ferredoxin reduction and proton/Na(+) translocating ferredoxin oxidation. Biochim Biophys Acta 1827(2):94–113.  https://doi.org/10.1016/j.bbabio.2012.07.002 CrossRefPubMedGoogle Scholar
  10. Buckel W, Thauer RK (2018a) Flavin-based electron bifurcation, a new mechanism of biological energy coupling. Chem Rev 118(7):3862–3886.  https://doi.org/10.1021/acs.chemrev.7b00707 CrossRefPubMedGoogle Scholar
  11. Buckel W, Thauer RK (2018b) Flavin-based Electron bifurcation, ferredoxin, flavodoxin, and anaerobic respiration with protons (Ech) or NAD+ (Rnf) as electron acceptors: a historical review. Front Microbiol 9:401.  https://doi.org/10.3389/fmicb.2018.00401 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cai G, Jin B, Monis P, Saint C (2013) A genetic and metabolic approach to redirection of biochemical pathways of Clostridium butyricum for enhancing hydrogen production. Biotechnol Bioeng 110(1):338–342.  https://doi.org/10.1002/bit.24596 CrossRefPubMedGoogle Scholar
  13. Cai G, Jin B, Saint C, Monis P (2011) Genetic manipulation of butyrate formation pathways in Clostridium butyricum. J Biotechnol 155(3):269–274.  https://doi.org/10.1016/j.jbiotec.2011.07.004 CrossRefPubMedGoogle Scholar
  14. Calusinska M, Happe T, Joris B, Wilmotte A (2010) The surprising diversity of clostridial hydrogenases: a comparative genomic perspective. Microbiology 156(Pt 6):1575–1588.  https://doi.org/10.1099/mic.0.032771-0 CrossRefPubMedGoogle Scholar
  15. Carere CR, Kalia V, Sparling R, Cicek N, Levin DB (2008) Pyruvate catabolism and hydrogen synthesis pathway genes of Clostridium thermocellum ATCC 27405. Indian J Microbiol 48(2):252–266.  https://doi.org/10.1007/s12088-008-0036-z CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chandel AK, Chandrasekhar G, Silva MB, Silverio da Silva S (2012) The realm of cellulases in biorefinery development. Crit Rev Biotechnol 32(3):187–202.  https://doi.org/10.3109/07388551.2011.595385 CrossRefPubMedGoogle Scholar
  17. Cohen J, Kim K, King P, Seibert M, Schulten K (2005) Finding gas diffusion pathways in proteins: application to O2 and H2 transport in CpI [FeFe]-hydrogenase and the role of packing defects. Structure 13(9):1321–1329.  https://doi.org/10.1016/j.str.2005.05.013 CrossRefPubMedGoogle Scholar
  18. Das D, Veziroglu TN (2008) Advances in biological hydrogen production processes. Int J Hydrog Energy 33:6046–6054CrossRefGoogle Scholar
  19. 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(1):113–121.  https://doi.org/10.1111/j.1574-6968.2007.00868.x CrossRefPubMedGoogle Scholar
  20. Dubini A, Ghirardi ML (2015) Engineering photosynthetic organisms for the production of biohydrogen. Photosynth Res 123(3):241–253.  https://doi.org/10.1007/s11120-014-9991-x CrossRefPubMedGoogle Scholar
  21. Ducat DC, Sachdeva G, Silver PA (2011) Rewiring hydrogenase-dependent redox circuits in cyanobacteria. Proc Natl Acad Sci U S A 108(10):3941–3946.  https://doi.org/10.1073/pnas.1016026108 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107(10):4273–4303.  https://doi.org/10.1021/cr050195z CrossRefPubMedGoogle Scholar
  23. Frey M (2002) Hydrogenases: hydrogen-activating enzymes. Chembiochem 3(2–3):153–160CrossRefGoogle Scholar
  24. Gauquelin C, Baffert C, Richaud P, Kamionka E, Etienne E, Guieysse D, Girbal L, Fourmond V, Andre I, Guigliarelli B, Leger C, Soucaille P, Meynial-Salles I (2018) Roles of the F-domain in [FeFe] hydrogenase. Biochim Biophys Acta 1859(2):69–77.  https://doi.org/10.1016/j.bbabio.2017.08.010 CrossRefGoogle Scholar
  25. Greening C, Biswas A, Carere CR, Jackson CJ, Taylor MC, Stott MB, Cook GM, Morales SE (2016) Genomic and metagenomic surveys of hydrogenase distribution indicate H2 is a widely utilised energy source for microbial growth and survival. ISME J 10(3):761–777.  https://doi.org/10.1038/ismej.2015.153 CrossRefPubMedGoogle Scholar
  26. Gupta SK, Kumari S, Reddy K, Bux F (2013) Trends in biohydrogen production: major challenges and state-of-the-art developments. Environ Technol 34(13–16):1653–1670.  https://doi.org/10.1080/09593330.2013.822022 CrossRefPubMedGoogle Scholar
  27. Hallenbeck PC (2005) Fundamentals of the fermentative production of hydrogen. Water Sci Technol 52(1–2):21–29CrossRefGoogle Scholar
  28. Hitit ZY, Lazaro CZ, Hallenbeck PC (2017) Hydrogen production by co-cultures of Clostridium butyricum and Rhodospeudomonas palustris: optimization of yield using response surface methodology. Int J Hydrog Energy 42:6578–6589CrossRefGoogle Scholar
  29. Hye JJ, Ok JC, Yoon LS, Sung LD, Moon PJ (2010) Molecular characterization and homologous overexpression of [FeFe]-hydrogenase in Clostridium tyrobutyricum JM1. Int J Hydrog Energy 35:1065–1073CrossRefGoogle Scholar
  30. Jiang L, Wu Q, Xu Q, Zhu L, Huang H (2017) Fermentative hydrogen production from Jerusalem artichoke by Clostridium tyrobutyricum expressing exo-inulinase gene. Sci Rep 7(1):7940.  https://doi.org/10.1038/s41598-017-07207-7 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Joseph RC, Kim NM, Sandoval NR (2018) Recent developments of the synthetic biology toolkit for Clostridium. Front Microbiol 9:154.  https://doi.org/10.3389/fmicb.2018.00154 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Khanna N, Lindblad P (2015) Cyanobacterial hydrogenases and hydrogen metabolism revisited: recent progress and future prospects. Int J Mol Sci 16(5):10537–10561.  https://doi.org/10.3390/ijms160510537 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Klein M, Ansorge-Schumacher MB, Fritscha M, Hartmeier M (2010) Influence of hydrogenase overexpression on hydrogen production of Clostridium acetobutylicum DSM 792. Enzym Microb Technol 46(5):384–390CrossRefGoogle Scholar
  34. Koo J, Shiigi S, Rohovie M, Mehta K, Swartz JR (2016) Characterization of [FeFe] hydrogenase O2 sensitivity using a new, physiological approach. J Biol Chem 291(41):21563–21570.  https://doi.org/10.1074/jbc.M116.737122 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Kothari R, Kumar V, Pathak VV, Ahmad S, Aoyi O, Tyagi VV (2017) A critical review on factors influencing fermentative hydrogen production. Front Biosci 22:1195–1220CrossRefGoogle Scholar
  36. Kpebe A, Benvenuti M, Guendon C, Rebai A, Fernandez V, Le Laz S, Etienne E, Guigliarelli B, Garcia-Molina G, de Lacey AL, Baffert C, Brugna M (2018) A new mechanistic model for an O2-protected electron-bifurcating hydrogenase, Hnd from Desulfovibrio fructosovorans. Biochim Biophys Acta in PressGoogle Scholar
  37. Kubas A, Orain C, De Sancho D, Saujet L, Sensi M, Gauquelin C, Meynial-Salles I, Soucaille P, Bottin H, Baffert C, Fourmond V, Best RB, Blumberger J, Leger C (2017) Mechanism of O2 diffusion and reduction in FeFe hydrogenases. Nat Chem 9(1):88–95.  https://doi.org/10.1038/nchem.2592 CrossRefPubMedGoogle Scholar
  38. Kumar G, Mudhoo A, Sivagurunathan P, Nagarajan D, Ghimire A, Lay CH, Lin CY, Lee DJ, Chang JS (2016) Recent insights into the cell immobilization technology applied for dark fermentative hydrogen production. Bioresour Technol 219:725–737CrossRefGoogle Scholar
  39. Lacasse MJ, Zamble DB (2016) [NiFe]-hydrogenase maturation. Biochemistry 55(12):1689–1701.  https://doi.org/10.1021/acs.biochem.5b01328 CrossRefPubMedGoogle Scholar
  40. Lee SF, Forsberg CW, Gibbins LN (1985) Cellulolytic activity of Clostridium acetobutylicum. Appl Environ Microbiol 50(2):220–228PubMedPubMedCentralGoogle Scholar
  41. Leroux F, Dementin S, Burlat B, Cournac L, Volbeda A, Champ S, Martin L, Guigliarelli B, Bertrand P, Fontecilla-Camps J, Rousset M, Leger C (2008) Experimental approaches to kinetics of gas diffusion in hydrogenase. Proc Natl Acad Sci U S A 105(32):11188–11193.  https://doi.org/10.1073/pnas.0803689105 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Levin DB, Islam R, Cicek N, Sparling R (2006) Hydrogen production by Clostridium thermocellum 27405 from cellulosic biomass substrates. Int J Hydrog Energy 31:1496–1503CrossRefGoogle Scholar
  43. Li F, Hinderberger J, Seedorf H, Zhang J, Buckel W, Thauer RK (2008) Coupled ferredoxin and crotonyl coenzyme A (CoA) reduction with NADH catalyzed by the butyryl-CoA dehydrogenase/Etf complex from Clostridium kluyveri. J Bacteriol 190(3):843–850.  https://doi.org/10.1128/JB.01417-07 CrossRefPubMedGoogle Scholar
  44. Liu X, Zhu Y, Yang ST (2006) Construction and characterization of ack deleted mutant of Clostridium tyrobutyricum for enhanced butyric acid and hydrogen production. Biotechnol Prog 22(5):1265–1275.  https://doi.org/10.1021/bp060082g CrossRefPubMedGoogle Scholar
  45. Lo Y, Chen C, Lee C, Chang JS (2010) Sequential dark-photo fermentation and autotrophic microalgal growth for high-yield and CO2-free biohydrogen production. Int J Hydrog Energy 35:10944–10953CrossRefGoogle Scholar
  46. Martin BA, Frymier PD (2017) A review of hydrogen production by photosynthetic organisms using whole-cell and cell-free systems. Appl Biochem Biotechnol 183(2):503–519.  https://doi.org/10.1007/s12010-017-2576-3 CrossRefPubMedGoogle Scholar
  47. Mitchell WJ (2016) Sugar uptake by the solventogenic clostridia. World J Microbiol Biotechnol 32, 32(2)Google Scholar
  48. Mizuno O, Dinsdale R, Hawkes FR, Hawkes DL, Noike T (2000) Enhancement of hydrogen production from glucose by nitrogen gas sparging. Bioresour Technol 73:59–65CrossRefGoogle Scholar
  49. Montet Y, Amara P, Volbeda A, Vernede X, Hatchikian EC, Field MJ, Frey M, Fontecilla-Camps JC (1997) Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics. Nat Struct Biol 4(7):523–526CrossRefGoogle Scholar
  50. 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(2):229–234.  https://doi.org/10.1016/j.femsle.2005.04.014 CrossRefPubMedGoogle Scholar
  51. Nakayama S, Kosaka T, Hirakawa H, Matsuura K, Yoshino S, Furukawa K (2008) Metabolic engineering for solvent productivity by downregulation of the hydrogenase gene cluster hupCBA in Clostridium saccharoperbutylacetonicum strain N1-4. Appl Microbiol Biotechnol 78(3):483–493.  https://doi.org/10.1007/s00253-007-1323-z CrossRefPubMedGoogle Scholar
  52. Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7(1):13–23CrossRefGoogle Scholar
  53. Nomura T, Naimen A, Toyoda S, Kuriyama Y, Tokumoto H, Konishi Y (2014) Isolation and characterization of a novel hydrogen-producing strain Clostridium sp. suitable for immobilization. Int J Hydrog Energy 39:1280–1287CrossRefGoogle Scholar
  54. Noth J, Kositzki R, Klein K, Winkler M, Haumann M, Happe T (2015) Lyophilization protects [FeFe]-hydrogenases against O2-induced H-cluster degradation. Sci Rep 5:13978.  https://doi.org/10.1038/srep13978 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Olson DG, McBride JE, Shaw AJ, Lynd LR (2012) Recent progress in consolidated bioprocessing. Curr Opin Biotechnol 23(3):396–405.  https://doi.org/10.1016/j.copbio.2011.11.026 CrossRefPubMedGoogle Scholar
  56. Orain C, Saujet L, Gauquelin C, Soucaille P, Meynial-Salles I, Baffert C, Fourmond V, Bottin H, Leger C (2015) Electrochemical measurements of the kinetics of inhibition of two FeFe hydrogenases by O2 demonstrate that the reaction is partly reversible. J Am Chem Soc 137(39):12580–12587.  https://doi.org/10.1021/jacs.5b06934 CrossRefPubMedGoogle Scholar
  57. Ozgur E, Mars AE, Peksel B, Louwerse A, Yucel M, Gunduz U, Claassen PAM, Eroglu I (2010) Biohydrogen production from beet molasses by sequential dark and photo-fermentation. Int J Hydrog Energy 35:511–517CrossRefGoogle Scholar
  58. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282(5395):1853–1858CrossRefGoogle Scholar
  59. Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, King PW, Adams MW (2015) [FeFe]- and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochim Biophys Acta 1853(6):1350–1369.  https://doi.org/10.1016/j.bbamcr.2014.11.021 CrossRefPubMedGoogle Scholar
  60. Plummer SM, Plummer MA, Merkel PA, Hagen M, Biddle JF, Waidner LA (2016) Using directed evolution to improve hydrogen production in chimeric hydrogenases from Clostridia species. Enzym Microb Technol 93-94:132–141.  https://doi.org/10.1016/j.enzmictec.2016.07.011 CrossRefGoogle Scholar
  61. Poudel S, Tokmina-Lukaszewska M, Colman DR, Refai M, Schut GJ, King PW, Maness PC, Adams MW, Peters JW, Bothner B, Boyd ES (2016) Unification of [FeFe]-hydrogenases into three structural and functional groups. Biochim Biophys Acta 1860(9):1910–1921.  https://doi.org/10.1016/j.bbagen.2016.05.034 CrossRefPubMedGoogle Scholar
  62. Rittmann S, Herwig C (2012) A comprehensive and quantitative review of dark fermentative biohydrogen production. Microb Cell Factories 11:115.  https://doi.org/10.1186/1475-2859-11-115 CrossRefGoogle Scholar
  63. Rotta C, Poehlein A, Schwarz K, McClure P, Daniel R, Minton NP (2015) Closed genome sequence of Clostridium pasteurianum ATCC 6013. Genome Announc 3(1).  https://doi.org/10.1128/genomeA.01596-14
  64. Sabathe F, Belaich A, Soucaille P (2002) Characterization of the cellulolytic complex (cellulosome) of Clostridium acetobutylicum. FEMS Microbiol Lett 217(1):15–22CrossRefGoogle Scholar
  65. Schuchmann K, Muller V (2012) A bacterial electron-bifurcating hydrogenase. J Biol Chem 287(37):31165–31171.  https://doi.org/10.1074/jbc.M112.395038 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Schut GJ, Adams MW (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191(13):4451–4457.  https://doi.org/10.1128/JB.01582-08 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Schwartz E, Fritsch J, Friedrich B (2013) H2-metabolizing prokaryotes. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes: prokaryotic physiology and biochemistry, 4th edn. Springer, Berlin, pp 119–199CrossRefGoogle Scholar
  68. Seelert T, Ghosh D, Yargeau V (2015) Improving biohydrogen production using Clostridium beijerinckii immobilized with magnetite nanoparticles. Appl Microbiol and Biotechnol 99(9):4107–4116.  https://doi.org/10.1007/s00253-015-6484-6 CrossRefGoogle Scholar
  69. Shepard EM, Mus F, Betz JN, Byer AS, Duffus BR, Peters JW, Broderick JB (2014) [FeFe]-hydrogenase maturation. Biochemistry 53(25):4090–4104.  https://doi.org/10.1021/bi500210x CrossRefPubMedGoogle Scholar
  70. Show KY, Zhang ZP, Lee DJ (2008) Design of bioreactors for biohydrogen production. J Sci Ind Res 67:941–949Google Scholar
  71. Tangney M, Mitchell WJ (2007) Characterisation of a glucose phosphotransferase system in Clostridium acetobutylicum ATCC 824. Appl Microbiol Biotechnol 74(2):398–405.  https://doi.org/10.1007/s00253-006-0679-9 CrossRefPubMedGoogle Scholar
  72. Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41(1):100–180PubMedPubMedCentralGoogle Scholar
  73. Therien JB, Artz JH, Poudel S, Hamilton TL, Liu Z, Noone SM, Adams MWW, King PW, Bryant DA, Boyd ES, Peters JW (2017) The physiological functions and structural determinants of catalytic bias in the [FeFe]-hydrogenases CpI and CpII of Clostridium pasteurianum strain W5. Front Microbiol 8:1305.  https://doi.org/10.3389/fmicb.2017.01305 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Thomas L, Joseph A, Gottumukkala LD (2014) Xylanase and cellulase systems of Clostridium sp.: an insight on molecular approaches for strain improvement. Bioresour Technol 158:343–350.  https://doi.org/10.1016/j.biortech.2014.01.140 CrossRefPubMedGoogle Scholar
  75. Vardar-Schara G, Maeda T, Wood TK (2008) Metabolically engineered bacteria for producing hydrogen via fermentation. Microb Biotechnol 1(2):107–125.  https://doi.org/10.1111/j.1751-7915.2007.00009.x CrossRefPubMedGoogle Scholar
  76. Verhaart MR, Bielen AA, van der Oost J, Stams AJ, Kengen SW (2010) Hydrogen production by hyperthermophilic and extremely thermophilic bacteria and archaea: mechanisms for reductant disposal. Environ Technol 31(8–9):993–1003CrossRefGoogle Scholar
  77. Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107(10):4206–4272.  https://doi.org/10.1021/cr050196r CrossRefPubMedGoogle Scholar
  78. Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25(4):455–501CrossRefGoogle Scholar
  79. Wang S, Huang H, Kahnt J, Mueller AP, Kopke M, Thauer RK (2013a) NADP-specific electron-bifurcating [FeFe]-hydrogenase in a functional complex with formate dehydrogenase in Clostridium autoethanogenum grown on CO. J Bacteriol 195(19):4373–4386.  https://doi.org/10.1128/JB.00678-13 CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wang S, Huang H, Kahnt J, Thauer RK (2013b) A reversible electron-bifurcating ferredoxin- and NAD-dependent [FeFe]-hydrogenase (HydABC) in Moorella thermoacetica. J Bacteriol 195(6):1267–1275.  https://doi.org/10.1128/JB.02158-12 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Xiong W, Reyes LH, Michener WE, Maness PC, Chou KJ (2018) Engineering cellulolytic bacterium Clostridium thermocellum to co-ferment cellulose- and hemicellulose-derived sugars simultaneously. Biotechnol Bioeng 115(7):1755–1763.  https://doi.org/10.1002/bit.26590 CrossRefPubMedGoogle Scholar
  82. Yokoi H, Saitsu A, Uchida H, Hirose J, Hayashi S, Takasaki Y (2001) Microbial hydrogen production from sweet potato starch residue. J Biosci Bioeng 91(1):58–63CrossRefGoogle Scholar
  83. Zhao X, Xing D, Fu N, Liu B, Ren N (2011) Hydrogen production by the newly isolated Clostridium beijerinckii RZF-1108. Bioresour Technol 102(18):8432–8436.  https://doi.org/10.1016/j.biortech.2011.02.086 CrossRefPubMedGoogle Scholar
  84. Zheng Y, Kahnt J, Kwon IH, Mackie RI, Thauer RK (2014) Hydrogen formation and its regulation in Ruminococcus albus: involvement of an electron-bifurcating [FeFe]-hydrogenase, of a non-electron-bifurcating [FeFe]-hydrogenase, and of a putative hydrogen-sensing [FeFe]-hydrogenase. J Bacteriol 196(22):3840–3852.  https://doi.org/10.1128/JB.02070-14 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.CNRS, LCB, Laboratoire de Chimie BactérienneAix-Marseille UniversityMarseilleFrance
  2. 2.CNRS, BIP, Bioénergétique et Ingénierie des ProtéinesAix-Marseille UniversityMarseilleFrance

Personalised recommendations