Skip to main content
SpringerLink
Log in
Book cover

Enzymes for Solving Humankind's Problems pp 247–273Cite as

Biological Production of Hydrogen

  • Chapter
  • First Online:

Abstract

The production of H2 from renewable sources, such as water or biomass, is a sustainable strategy for energy supply. Hydrogenases are the only enzymes that specifically catalyze the reversible reaction of H2 production/uptake with almost no overpotential. In this chapter, we review the advances produced in the last decade in the biocatalytic production of H2, including systems based on isolated hydrogenases as well as those using microorganisms through dark fermentation processes.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Navarro RM, Peña MA, Fierro JLG (2007) Hydrogen production reactions from carbon feedstocks: fossil fuels and biomass. Chem Rev 107:4304–4330

    Article  CAS  Google Scholar 

  2. De Lacey AL, Fernandez VM, Rousset M, Cammack R (2007) Activation and inactivation of hydrogenase function and the catalytic cycle: spectroelectrochemical studies. Chem Rev 107:4304–4330

    Article  PubMed  CAS  Google Scholar 

  3. Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107:4273–4303

    Article  CAS  PubMed  Google Scholar 

  4. Murphy BJ, Sargent F, Armstrong FA (2014) Transforming an oxygen-tolerant NiFe uptake hydrogenase into a proficient, reversible hydrogen producer. Energy Environ Sci 7:1426–1433

    Article  CAS  Google Scholar 

  5. Hexter SV, Grey F, Happe T, Climent V, Armstrong FA (2012) Electrocatalytic mechanism of reversible hydrogen cycling by enzymes and distinctions between the major classes of hydrogenases. Proc Natl Acad Sci USA 109:18232–18233

    Article  CAS  Google Scholar 

  6. Fourmond V, Baffert C, Sybirna K, Dementin S, Abou-Hamdan A, Meynial-Salles I, Soucaille P, Bottin H, Leger C (2013) The mechanism of inhibition by H2 of H2-evolution by hydrogenases. Chem Commun 49:6840–6842

    Article  CAS  Google Scholar 

  7. Kubas A, De Sancho D, Best RB, Blumberger J (2014) Aerobic damage to FeFe-hydrogenases: activation barriers for the chemical attachment of O2. Angew Chem Int Ed 53:4081–4084

    Article  CAS  Google Scholar 

  8. Lu Y, Koo J (2019) O2 sensitivity and H2 production activity of hydrogenases—a review. Biotechnol Bioeng 116:3124–3135

    Article  CAS  PubMed  Google Scholar 

  9. Roseboom W, DeLacey AL, Fernandez VM, Hatchikian EC, Albracht SPJ (2006) The active site of the [FeFe]-hydrogenase from Desulfovibrio desulfuricans. II. Redox properties, light sensitivity and CO-ligand exchange as observed by infrared spectroscopy. J Biol Inorg Chem 11:102–118

    Article  CAS  PubMed  Google Scholar 

  10. Zorin NA, Gogotov IN, Kondratieva EN (1979) Hydrogen production by hydrogenase of Alcaligenes eutrophus z-1 in the presence of oxygen. FEMS Microbiol Lett 5:301–304

    Article  CAS  Google Scholar 

  11. Horch M, Lauterbach L, Mroginski MA, Hildebrandt P, Lenz O, Zebger I (2015) Reversible active site sulfoxygenation can explain the oxygen tolerance of a NAD+-reducing [NiFe] hydrogenase and its unusual infrared spectroscopic properties. J Am Chem Soc 137:2555–2564

    Article  CAS  PubMed  Google Scholar 

  12. Inoue T, Kumar SN, Kamachi T, Okura I (1999) Hydrogen evolution from glucose with the combination of glucose dehydrogenase and hydrogenase from A-eutrophus H16. Chem Lett 147–148

    Google Scholar 

  13. Zhang YHP, Evans BR, Mielenz JR, Hopkins RC, Adams MWW (2007) High-yield hydrogen production from starch and water by a synthetic enzymatic pathway. PLoS ONE 2:e456

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Smith PR, Bingham AS, Swartz JR (2012) Generation of hydrogen from NADPH using an [FeFe] hydrogenase. Int J Hydrogen Energy 37:2977–2983

    Article  CAS  Google Scholar 

  15. Lu F, Smith FR, Mehta K, Swartz JR (2015) Development of a synthetic pathway to convert glucose to hydrogen using cell fre extracts. Int J Hydrogen Energy 40:9113–9124

    Article  CAS  Google Scholar 

  16. Mateo C, Palomo JM, Fernandez-Lorente G, Guisan JM, Fernandez-Lafuente R (2007) Improvement of enzyme activity, stability and selectivity via immobilization technique. Enzym Microb Technol 40:1451–1463

    Article  CAS  Google Scholar 

  17. Zadvorny OA, Barrows AM, Zorin NA, Peters JW, Elgren TE (2010) High level of hydrogen production activity achieved for hydrogenase encapsulated in sol-gel material doped with carbon nanotubes. J Mater Chem 20:1065–1067

    Article  CAS  Google Scholar 

  18. Baker SE, Hopkins RC, Blanchette CD, Walsworth VL, Sumbad R, Fischer NO, Kuhn EA, Coleman M, Chromy BA, Letant SE, Hoeprich PD, Adams MWW, Henderson PT (2009) Hydrogen production by a hyperthermophilic membrane-bound hydrogenase in water-soluble nanolipoprotein particles. J Am ChemSoc 131:7508–7509

    Article  CAS  Google Scholar 

  19. Jordan PC, Patterson DP, Saboda KN, Edwards EJ, Miettinen HM, Basu G, Thielges MC, Douglas T (2016) Self-assembling biomolecular catalysts for hydrogen production. Nat Chem 8:179–185

    Article  CAS  PubMed  Google Scholar 

  20. Baltazar CSA, Marques MC, Soares CM, DeLacey AM, Pereira IAC, Matias PM (2011) Nickel-iron-selenium hydrogenases—an overview. Eur J Inorg Chem 948–962

    Google Scholar 

  21. Valente FMA, Oliveira ASF, Gnadt N, Pacheco I, Coelho AV, Xavier AV, Teixeira M, Soares CM, Pereira IAC (2005) Hydrogenases in Desulfovibrio vulgaris Hildenborough: Structural and physiologic characterisation of the membrane-bound [NiFeSe] hydrogenase. J Biol Inorg Chem 10:667–682

    Article  CAS  PubMed  Google Scholar 

  22. Stein M, Lubitz W (2001) The electronic structure of the catalytic intermediate Ni-C in [NiFe] and [NiFeSe] hydrogenases. Phys Chem Chem Phys 3:5115–5120

    Article  CAS  Google Scholar 

  23. Parkin A, Goldet G, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2008) The difference a Se makes? Oxygen-tolerant hydrogen production by the [NiFeSe]-hydrogenase from Desulfomicrobium baculatum. J Am Chem Soc 130:13410–13416

    Article  CAS  PubMed  Google Scholar 

  24. Gutiérrez-Sánchez C, Rüdiger O, Fernández VM et al (2010) Interaction of the active site of the Ni-Fe-Se hydrogenase from Desulfovibrio vulgaris Hildenborough with carbon monoxide and oxygen inhibitors. J Biol Inorg Chem 15:1285–1292

    Article  PubMed  CAS  Google Scholar 

  25. Maroney MJ, Hondal RJ (2018) Selenium versus sulfur: reversibility of chemical reactions and resistant to permanent oxidation in proteins and nucleic acids. Free Radical Biol Med 127:228–237

    Article  CAS  Google Scholar 

  26. Marques MC, Coelho R, De Lacey AL, Pereira IAC, Matias PM (2010) The three-dimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough: a hydrogenase without a bridging ligand in the active site in its oxidised, “as-isolated” state. J Mol Biol 396:893–907

    Article  CAS  PubMed  Google Scholar 

  27. Marques MC, Tapia C, Gutierrez-Sanz O, Ramos AR, Keller KL, Wall JD, De Lacey AL, Matias PM, Pereira IAC (2017) The direct role of selenocysteine in NiFeSe hydrogenase maturation and catalysis. Nat Chem Biol 13:544–550

    Article  CAS  PubMed  Google Scholar 

  28. Zacarias S, Temporao A, Del Barrio M, Fourmond V, Leger C, Matias PM, Pereira IAC (2019) A hydrophillic channel is involved in oxidative inactivation of a [NiFeSe] hydrogenase. ACS Catal 9:8509–8519

    Article  CAS  Google Scholar 

  29. Plummer SM, Plummer MA, Merkel P, Hagen M, Biddle J, Waidner L (2016) Using directed evolution to improve hydrogen production in chimeric hydrogenases from Clostridia species. Enzym Microb Technol 93:132–141

    Article  CAS  Google Scholar 

  30. Koo J, Schabel T, liong S, Evitt NH, Swartz JR, (2017) High-throughput screening of catalytic H2 production. Angew Chem Int Ed 56:1012–1016

    Article  CAS  Google Scholar 

  31. Armstrong FA, Belsey NA. Cracknell JA, Goldet G, Parkin A, Reisner E, Vincent KA, Wait AF (2009) Dynamic electrochemical investigations of hydrogen oxidation and production by enzymes and implications for future technology. Chem Soc Rev 38:36–51

    Google Scholar 

  32. Vincent K, Parkin A, Armstrong FA (2007) Investigating and exploiting the electrocatalytic properties of hydrogenases. Chem Rev 107:4366–4413

    Article  CAS  PubMed  Google Scholar 

  33. Hexter SV, Chung MW, Vincent KA, Armstrong FA (2014) Unusual reaction of NiFe-hydrogenases with cyanide. J Am Chem Soc 136:10470–10477

    Article  CAS  PubMed  Google Scholar 

  34. Fourmond V, Lautier T, Baffert C, Leroux F, Liebgott PP, Dementin S, Rousset M, Arnoux P, Pignol D, Meynial-Salles I, Soucaille P, Bertrand P, Leger C (2009) Correcting for electrocatalyst desorption and inactivation in chronoamperometry experiments. Anal Chem 81:2962–2968

    Article  CAS  PubMed  Google Scholar 

  35. Krassen H, Stripp S, von Abendroth G, Ataka K, Happe T, Heberle J (2009) Immobilization of the [FeFe]-hydrogenase CrHydA1 on a gold electrode: design of a catalytic surface for the production of molecular hydrogen. J Biotechnol 142:3–9

    Article  CAS  PubMed  Google Scholar 

  36. Kihara T, Liu XY, Nakamura C, Park KM, Han SW, Qian DJ, Kawasaki K, Zorin NA, Yasuda S, Hata K, Wakayama T, Miyake J (2011) Direct electron transfer to hydrogenase for catalytic hydrogen production using a single-walled carbon nanotube forest. Int J Hydrogen Energy 36:7523–7529

    Article  CAS  Google Scholar 

  37. Morra S, Valetti F, Sarasso V, Castrignano S, Sadeghi SJ, Gilardi G (2015) Hydrogen production at high faradaic efficiency by a bio-electrode based on TiO2 adsorption of a new FeFe-hydrogenase from Clostridium perfringens. Bioelectrochemistry 106:258–262

    Article  CAS  PubMed  Google Scholar 

  38. Schlicht S, Assaud L, Hansen M, Licklederer M, Bechelany M, Perner M, Bachmann J (2016) An electrochemically functional layer of hydrogenase extract on an electrode of large and tunable specific surface area. J Mater Chem A 4:6487–6494

    Article  CAS  Google Scholar 

  39. Shiraiwa S, So K, Sugimoto Y, Kitazumi Y, Shirai O, Nishikawa K, Higuchi Y, Kano K (2018) Reactivation of standard [NiFe]-hydrogenase and bioelectrochemical catalysis of proton reduction and hydrogen oxidation in a mediated-electron-transfer system. Bioelectrochemistry 123:156–161

    Article  CAS  PubMed  Google Scholar 

  40. Wakerley DW, Reisner E (2015) Oxygen tolerant proton reduction catalysis: much O2 about nothing. Energy Environ Sci 8:2283–2295

    Article  CAS  Google Scholar 

  41. Gutiérrez-Sanz O, Tapia C, Marques MC, Zacarías S, Vélez M, Pereira IAC, De Lacey AL (2015) Induction of a proton gradient across a gold-supported biomimetic membrane by electroenzymatic H2 oxidation. Angew Chem Int Ed 54:2684–2687

    Article  CAS  Google Scholar 

  42. Rodriguez-Macia P, Birrell J, Lubitz W, Rüdiger O (2017) Electrochemical investigations on the inactivation of the [FeFe] hydrogenase from Desulfovibrio desulfuricans by O2 or light under hydrogen-producing conditions. ChemPlusChem 82:540–545

    Article  CAS  PubMed  Google Scholar 

  43. Caserta G, Papini C, Adamska-Venkatesh A, Pecqueur L, Sommer C, Reijerse E, Lubitz W, Gauquelin C, Meynial-Salles I, Pramanik D, Artero V, Atta M, del Barrio M, Faivre B, Fourmond V, Leger C, Fontecave M (2018) Engineering an FeFe-hydrogenase: do accessory clusters influence O2 resistance and catalytic bias? J Am Chem Soc 140:5516–5526

    Article  CAS  PubMed  Google Scholar 

  44. Reisner E, Fontecilla-Camps JC, Armstrong FA (2009) Catalytic electrochemistry of a [NiFeSe]-hydrogenase on TiO2 and demonstration of its suitability for visible-light driven H2 production. Chem Commun 550–552

    Google Scholar 

  45. Reisner E, Powell DJ, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2009) Visible light-driven h2 production by hydrogenases attached to dye-sensitized TiO2 nanoparticles. J Am Chem Soc 131:18457–18466

    Article  CAS  PubMed  Google Scholar 

  46. Brown KA, Dayal S, Ai X, Rumbles G, King PW (2010) Controlled assembly of hydrogenase-CdTe nanocrystal hybrids for solar hydrogen production. J Am Chem Soc 132:9672–9680

    Article  CAS  PubMed  Google Scholar 

  47. Greene BL, Joseph CA, Maroney MJ, Dyer RB (2012) Direct evidence of active-site reduction and photodriven catalysis in sensitized hydrogenase assemblies. J Am Chem Soc 134:11108–11111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Sakai T, Mersch D, Reisner E (2013) Photocatalytic hydrogen evolution with a hydrogenase in a mediator-free system under high levels of oxygen. Angew Chem Int Ed 52:12313–12316

    Article  CAS  Google Scholar 

  49. Caputo CA, Gross MA, Lau VW, Cavazza C, Lotsch BV, Reisner E (2014) Photocatalytic hydrogen production using polymeric carbon nitride with a hydrogenase and a bioinspired synthetic Ni catalyst. Angew Chem Int Ed 53:11538–11542

    Article  CAS  Google Scholar 

  50. Caputo CA, Wang L, Beranek R, Reisner E (2015) Carbon nitride-TiO2 hybrid modified with hydrogenase for visible light driven hydrogen production. Chem Sci 6:5690–5694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Zhang L, Beaton SE, Carr SB, Armstrong FA (2018) Direct visible light activation of a surface cysteine-engineered [NiFe]-hydrogenase by silver nanoclusters. Energy Environ Sci 11:3342–3348

    Article  CAS  Google Scholar 

  52. Tapia C, Zacarias S, Pereira IAC, Conesa JC, Pita M, De Lacey AL (2016) In situ determination of photobioproduction of H2 by In2S3-[NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough using only visible light. ACS Catal 6:5691–5698

    Article  CAS  Google Scholar 

  53. Brown K, Wilker MB, Boehm M, Dukovic G, King PW (2012) Characterization of photochemical processes for H2 production by CdS nanorod-[FeFe] hydrogenase complexes. J Am Chem Soc 134:5627–5636

    Article  CAS  PubMed  Google Scholar 

  54. Wilker MB, Utterback JK, Greene S, Brown KA, Mulder DW, King PW, Dukovic G (2018) Role of surface-capping ligands in photoexcited electron transfer between CdS Nanorods and [FeFe] Hydrogenase subsequent H2 generation. J Phys Chem C 122:741–750

    Article  CAS  Google Scholar 

  55. Bae S, Shim E, Yoon J, Joo H (2008) Photoanodic and cathodic role of anodized tubular titania in light-sensitized enzymatic hydrogen production. J Power Sources 185:439–444

    Article  CAS  Google Scholar 

  56. Zhao Y, Anderson NC, Ratzloff MW, Mulder DW, Zhu K, Turner JA, Neale NR, King PW, Branz HM (2016) Proton reduction using a hydrogenase-modified nanoporous black silicon photoelectrode. ACS Appl Mater Interf 8:14481–14487

    Article  CAS  Google Scholar 

  57. Lee CY, Park HS, Fontecilla-Camps JC, Reisner E (2016) Photoelectrochemical H2 evolution with a hydrogenase immobilized on a TiO2-protected silicon electrode. Angew Chem Int Ed 55:5971–5974

    Article  CAS  Google Scholar 

  58. Moore EE, Andrei V, Zacarias S, Pereira IAC, Reisner, (2020) Integration of a hydrogenase in a head halide perovskite photoelectrode for tandem solar water splitting. ACS Energy Lett 5:232–237

    Article  CAS  Google Scholar 

  59. Tian L, Németh B, Berggren G, Tian H (2018) Hydrogen evolution by a photoelectrochemical cell based on a Cu2O-ZnO-[FeFe] hydrogenase electrode. J Photochem Photobiol a: Chem 366:27–33

    Article  CAS  Google Scholar 

  60. Tapia C, Milton RD, Pankratova G, Minteer SD, Akerlund HE, Leech D, De Lacey AL, Pita M, Gorton L (2017) Wiring of photosystem I and hydrogenase on an electrode for photoelectrochemical H2 production by using redox polymers for relatively positive onset potential. ChemelectroChem 4:90–95

    Article  CAS  Google Scholar 

  61. Zhao F, Wang P, Ruff A, Hartmann V, Zacarias S, Pereira IAC, Nowaczyk MM, Rögner M, Conzuelo F, Schuhmann W (2019) A photosystem I monolayer with anisotropic electron flow enables Z-scheme like photosynthetic water splitting. Energy Environ Sci 12:3133–3143

    Article  CAS  Google Scholar 

  62. Boodhun BSF, Mudhoo A, Kumar G, Kim SH, Lin CY (2017) Research perspectives on constraints, prospects and opportunities in biohydrogen production. Int J Hydrogen Energy 42:27471–27481

    Article  CAS  Google Scholar 

  63. Gopalakrishnan B, Khanna N, Das D (2019) Dark-fermentative biohydrogen production. In: Pandey A, Mohan SV, Chang JS, Hallenbeck PC, Larroche C (eds) Biohydrogen, 2nd edn. Elsevier, Amsterdam, pp 79–102

    Chapter  Google Scholar 

  64. Mishra P, Krishnan S, Rana S, Singh L, Sakinah M, Ab Wahid Z (2019) Outlook of fermentative hydrogen production techniques: an overview of dark, photo and integrated dark-photo fermentative approach to biomass. Energy Strateg Rev 24:27–37

    Article  Google Scholar 

  65. Stephen AJ, Archer SA, Orozco RL, Macaskie LE (2017) Advances and bottlenecks in microbial hydrogen production. Microb Biotechnol 10:1120–1127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Wang J, Yin Y (2019) Progress in microbiology for fermentative hydrogen production from organic wastes. Crit Rev Environ Sci Technol 49:825–865

    Article  CAS  Google Scholar 

  67. Kim DH, Kim MS (2011) Hydrogenases for biological hydrogen production. Bioresour Technol 102:8423–8431

    Article  CAS  PubMed  Google Scholar 

  68. Lubitz W, Ogata H, Rüdiger O, Reijerse E (2014) Hydrogenases. Chem Rev 114:4081–4148

    Article  CAS  PubMed  Google Scholar 

  69. Banu JR, Kavitha S, Kannah RY, Bhosale RR, Kumar G (2020) Industrial wastewater to biohydrogen: possibilities towards successful biorefinery route. Bioresour Technol 298:122378

    Article  CAS  Google Scholar 

  70. Srivastava N, Srivastava M, Malhotra BD, Gupta VK, Ramteke PW, Silva RN, Shukla P, Dubey KK, Mishra PK (2019) Nanoengineered cellulosic biohydrogen production via dark fermentation: a novel approach. Biotechnol Adv 37:107384

    Article  CAS  PubMed  Google Scholar 

  71. Trchounian K, Sawers RG, Trchounian A (2017) Improving biohydrogen productivity by microbial dark- and photo-fermentations: Novel data and future approaches. Renew Sustain Energy Rev 80:1201–1216

    Article  CAS  Google Scholar 

  72. Latifi A, Avilan L, Brugna M (2019) Clostridial whole cell and enzyme systems for hydrogen production: current state and perspectives. Appl Microbiol Biotechnol 103:567–575

    Article  CAS  PubMed  Google Scholar 

  73. Seol E, Kim S, Raj SM, Park S (2008) Comparison of hydrogen-production capability of four different Enterobacteriaceae strains under growing and non-growing conditions. Int J Hydrogen Energy 33:5169–5175

    Article  CAS  Google Scholar 

  74. Hallenbeck PC, Abo-Hashesh M, Ghosh D (2012) Strategies for improving biological hydrogen production. Bioresour Technol 110:1–9

    Article  CAS  PubMed  Google Scholar 

  75. Magnusson L, Cicek N, Sparling R, Levin D (2009) Continuous hydrogen production during fermentation of a cellulose by the thermophillic bacterium Clostridium thermocellum. Biotechnol Bioeng 102:759–766

    Article  CAS  PubMed  Google Scholar 

  76. Akhtar MK, Jones PR (2009) Construction of a synthetic YdbK-dependent pyruvate : H2 pathway in Escherichia coli BL21 ( DE3). Metab Eng 11:139–147

    Article  CAS  PubMed  Google Scholar 

  77. 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

    Article  CAS  PubMed  Google Scholar 

  78. 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 115:1755–1763

    Article  CAS  PubMed  Google Scholar 

  79. Sharma Y, Li B (2010) Optimizing energy harvest in wastewater treatment by combining anaerobic hydrogen producing biofermentor ( HPB ) and microbial fuel cell (MFC). Int J Hydrogen Energy 35:3789–3797

    Article  CAS  Google Scholar 

  80. Zhang Y, Liu M, Zhou M, Yang H, Liang L, Gu T (2019) Microbial fuel cell hybrid systems for wastewater treatment and bioenergy production: Synergistic effects, mechanisms and challenges. Renew Sustain Energy Rev 103:13–29

    Article  CAS  Google Scholar 

  81. Özgür E, Mars AE, Peksel B, Louwerse A, Yücel M, Gündüz U, Claassen PA, Eroğlu İ (2010) Biohydrogen production from beet molasses by sequential dark and photofermentation. Int J Hydrogen Energy 35:511–517

    Article  CAS  Google Scholar 

  82. Mishra P, Thakur S, Singh L, Ab Wahid Z, Sakinah M (2016) Enhanced hydrogen production from palm oil mill effluent using two stage sequential dark and photo fermentation. Int J Hydrogen Energy 41:18431–18440

    Article  CAS  Google Scholar 

  83. Morsy FM (2017) Synergistic dark and photo-fermentation continuous system for hydrogen production from molasses by Clostridium acetobutylicum ATCC 824 and Rhodobacter capsulatus DSM 1710. J Photochem Photobiol B Biol 169:1–6

    Article  CAS  Google Scholar 

  84. Zagrodnik R, Łaniecki M (2017) Hydrogen production from starch by co-culture of Clostridium acetobutylicum and Rhodobacter sphaeroides in one step hybrid dark- and photofermentation in repeated fed-batch reactor. Bioresour Technol 224:298–306

    Article  CAS  PubMed  Google Scholar 

  85. Laurinavichene T, Laurinavichius K, Shastik E, Tsygankov A (2017) Long-term H2 photoproduction from starch by co-culture of Clostridium butyricum and Rhodobacter sphaeroides in a repeated batch process. Biotechnol Lett 40:309–314

    Article  PubMed  CAS  Google Scholar 

  86. 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 219:725–737

    Article  CAS  PubMed  Google Scholar 

  87. Singh L, Wahid ZA, Siddiqui MF, Ahmad A, Rahim MHA, Sakinah M (2013) Biohydrogen production from palm oil mill effluent using immobilized Clostridium butyricum EB6 in polyethylene glycol. Process Biochem 48:294–298

    Article  CAS  Google Scholar 

  88. Rai PK, Singh SP, Asthana RK (2012) Biohydrogen production from cheese whey wastewater in a two-step anaerobic process. Appl Biochem Biotechnol 167:1540–1549

    Article  CAS  PubMed  Google Scholar 

  89. Kumar G, Mathimani T, Rene ER, Pugazhendhi A (2019) Application of nanotechnology in dark fermentation for enhanced biohydrogen production using inorganic nanoparticles. Int J Hydrogen Energy 44:13106–13113

    Article  CAS  Google Scholar 

  90. Taherdanak M, Zilouei H, Karimi K (2016) The effects of Fe0 and Ni0 nanoparticles versus Fe2+ and Ni2+ ions on dark hydrogen fermentation. Int J Hydrogen Energy 41:167–173

    Article  CAS  Google Scholar 

  91. Lim JK, Bae SS, Kim TW, Lee JH, Lee HS, Kang SG (2012) Thermodynamics of formate-oxidizing metabolism and implications for H2 production. Appl Environ Microbiol 78:7393–7397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Zilouei H, Taherdanak M (2015) Biohydrogen from lignocellulosic wastes. In: Karimi K (ed) Lignocellulose-based bioproducts. Springer, Heidelberg, pp 253–288

    Chapter  Google Scholar 

  93. Elreedy A, Ibrahim E, Hassan N, El-Dissouky A, Fujii M, Yoshimura C, Tawfik A (2017) Nickel-graphene nanocomposite as a novel supplement for enhancement of biohydrogen production from industrial wastewater containing mono-ethylene glycol. Energy Convers Manag 140:133–144

    Article  CAS  Google Scholar 

  94. Zhao Y, Chen Y (2011) Nano-TiO2 enhanced photofermentative hydrogen produced from the dark fermentation liquid of waste activated sludge. Environ Sci Technol 45:8589–8595

    Article  CAS  PubMed  Google Scholar 

  95. Fukuyama Y, Inoue M, Omae K, Yoshida T, Sako Y (2020) Anaerobic and hydrogenogenic carbon monoxide-oxidizing prokaryotes: versatile microbial conversion of a toxic gas into an available energy. Adv Appl Microbiol (in press)

    Google Scholar 

  96. Kottenhahn P, Schuchmann K, Müller V (2018) Efficient whole cell biocatalyst for formate-based hydrogen production. Biotechnol Biofuels 11:1–9

    Article  CAS  Google Scholar 

  97. Müller V (2019) New horizons in acetogenic conversion of one-carbon substrates and biological hydrogen storage. Trends Biotechnol 37:1344–1354

    Article  PubMed  CAS  Google Scholar 

  98. Eppinger J, Huang KW (2017) Formic acid as a hydrogen energy carrier. ACS Energy Lett 2:188–195

    Article  CAS  Google Scholar 

  99. Boddien A, Gärtner F, Federsel C, Sponholz P, Mellmann D, Jackstell R, Junge H, Beller M (2011) CO2-“neutral” hydrogen storage based on bicarbonates and formates. Angew Chem Int Ed 50:6411–6414

    Article  CAS  Google Scholar 

  100. Enthaler S, von Langermann J, Schmidt T (2010) Carbon dioxide and formic acid—the couple for environmental-friendly hydrogen storage? Energy Environ Sci 3:1207

    Article  CAS  Google Scholar 

  101. Jhong HRM, Ma S, Kenis PJA (2013) Electrochemical conversion of CO2 to useful chemicals: current status, remaining challenges, and future opportunities. Curr Opin Chem Eng 2:191–199

    Article  Google Scholar 

  102. Rittmann SKMR, Lee HS, Lim JK, Kim TW, Lee JH, Kang SG (2015) One-carbon substrate-based biohydrogen production: microbes, mechanism, and productivity. Biotechnol Adv 33:165–177

    Article  CAS  PubMed  Google Scholar 

  103. Pakes WCC, Jollyman WH (1901) The collection and examination o f the gases produced by bacteria. J Chem Soc Trans 79:322–329

    Article  CAS  Google Scholar 

  104. Pinske C, Sargent F (2016) Exploring the directionality of Escherichia coli formate hydrogenlyase: a membrane-bound enzyme capable of fixing carbon dioxide to organic acid. Microbiology (United Kingdom) 5:721–737

    CAS  Google Scholar 

  105. Yoshida A, Nishimura T, Kawaguchi H, Inui M, Yukawa H (2005) Enhanced hydrogen production from formic acid by formate hydrogen lyase-overexpressing Escherichia coli strains. Appl Environ Microbiol 71:6762–6768

    Google Scholar 

  106. Maeda T, Sanchez-Torres V, Wood TK (2012) Hydrogen production by recombinant Escherichia coli strains. Microb Biotechnol 5:214–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Yoshida A, Nishimura T, Kawaguchi H, Inui M, Yukawa H (2007) Efficient induction of formate hydrogen lyase of aerobically grown Escherichia coli in a three-step biohydrogen production process. Appl Microbiol Biotechnol 74:754–760

    Article  CAS  PubMed  Google Scholar 

  108. Kim S, Seol E, Mohan Raj S, Park S, Oh YK, Ryu DDY (2008) Various hydrogenases and formate-dependent hydrogen production in Citrobacter amalonaticus Y19. Int J Hydrogen Energy 33:1509–1515

    Article  CAS  Google Scholar 

  109. Shin JH, Yoon JH, Lee SH, Park TH (2010) Hydrogen production from formic acid in pH-stat fed-batch operation for direct supply to fuel cell. Bioresour Technol 101:53–58

    Article  CAS  Google Scholar 

  110. Martins M, Pereira IAC (2013) Sulfate-reducing bacteria as new microorganisms for biological hydrogen production. Int J Hydrogen Energy 38:12294–12301

    Article  CAS  Google Scholar 

  111. Martins M, Mourato C, Pereira IAC (2015) Desulfovibrio vulgaris growth coupled to formate-driven H2 production. Environ Sci Technol 49:14655–14662

    Article  CAS  PubMed  Google Scholar 

  112. Martins M, Mourato C, Morais-Silva FO, Rodrigues-Pousada C, Voordouw G, Wall JD, Pereira IAC (2016) Electron transfer pathways of formate-driven H2 production in Desulfovibrio. Appl Microbiol Biotechnol 100:8135–8146

    Article  CAS  PubMed  Google Scholar 

  113. Bae SS, Kim TW, Lee HS, Kwon KK, Kim YJ, Kim MS, Lee JH, Kang SG (2012) H2 production from CO, formate or starch using the hyperthermophilic archaeon. Thermococcus Onnurineus Biotechnol Lett 34:75–79

    Article  CAS  PubMed  Google Scholar 

  114. Bae SS, Lee HS, Jeon JH, Lee JH, Kang SG, Kim TW (2015) Enhancing bio-hydrogen production from sodium formate by hyperthermophilic archaeon, thermococcus onnurineus NA1. Bioprocess Biosyst Eng 38:989–993

    Article  CAS  PubMed  Google Scholar 

  115. Kim YJ, Lee HS, Kim ES, Bae SS, Lim JK, Matsumi R, Lebedinsky AV, Sokolova TG, Kozhevnikova DA, Cha SS, Kim SJ, Kwon KK, Imanaka T, Atomi H, Bonch-Osmolovskaya EA, Lee JH, Kang SG (2010) Formate-driven growth coupled with H2 production. Nature 467:352–355

    Article  CAS  PubMed  Google Scholar 

  116. Schuchmann K, Muller V (2013) Direct and reversible hydrogenation of CO2 to formate by a bacterial carbon dioxide reductase. Science 342:1382–1386

    Article  CAS  PubMed  Google Scholar 

  117. Alfano M, Cavazza C (2018) The biologically mediated water–gas shift reaction: structure, function and biosynthesis of monofunctional [NiFe]-carbon monoxide dehydrogenases. Sustain Energy Fuels 2:1653–1670

    Article  CAS  Google Scholar 

  118. Uffen RL (1976) Anaerobic growth of a Rhodopseudomonas species in the dark with carbon monoxide as sole and energy substrate. Proc Natl Acad Sci USA 73:3298–3302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Ainala SK, Seol E, Sekar BS, Park S (2014) Improvement of carbon monoxide-dependent hydrogen production activity in Citrobacter amalonaticus Y19 by over-expressing the CO-sensing transcriptional activator, CooA. Int J Hydrogen Energy 39:10417–10425

    Article  CAS  Google Scholar 

  120. Zhao Y, Haddad M, Cimpoia R, Liu Z, Guiot SR (2013) Performance of a Carboxydothermus hydrogenoformans-immobilizing membrane reactor for syngas upgrading into hydrogen. Int J Hydrogen Energy 38:2167–2175

    Article  CAS  Google Scholar 

  121. Kim MS, Bae SS, Kim YJ, Kim TW, Lim JK, Lee SH, Choi AR, Jeon JH, Lee JH, Lee HS, Kang SG (2013) CO-dependent H2 production by genetically engineered Thermococcus onnurineus NA1. Appl Environ Microbiol 79:2048–2053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Sokolova TG, Jeanthon C, Kostrikina NA, Chernyh NA, Lebedinsky AV, Stackebrandt E, Bonch-Osmolovskaya EA (2004) The first evidence of anaerobic CO oxidation coupled with H2 production by a hyperthermophilic archaeon isolated from a deep-sea hydrothermal vent. Extremophiles 8:317–323

    Article  CAS  PubMed  Google Scholar 

  123. Mohr T, Aliyu H, Küchlin R, Polliack S, Zwick M, Neumann A, Cowan D, Maayer P (2018) CO-dependent hydrogen production by the facultative anaerobe Parageobacillus thermoglucosidasius. Microb Cell Fact 17:1–12

    Article  CAS  Google Scholar 

  124. Sinharoy A, Baskaran D, Pakshirajan K (2019) Sustainable biohydrogen production by dark fermentation using carbon monoxide as the sole carbon and energy source. Int J Hydrogen Energy 44:13114–13125

    Article  CAS  Google Scholar 

  125. Sinharoy A, Pakshirajan K (2020) A novel application of biologically synthesized nanoparticles for enhanced biohydrogen production and carbon monoxide bioconversion. Renew Energy 147:864–873

    Article  CAS  Google Scholar 

  126. Ismail KSK, Najafpour G, Younesi H, Mohamed AR, Kamaruddin AH (2008) Biological hydrogen production from CO: bioreactor performance. Biochem Eng J 39:468–477

    Article  CAS  Google Scholar 

  127. Kim MS, Choi AR, Lee SH, Jung HC, Bae SS, Yang TJ, Jeon JH, Lim JK, Youn H, Kim TW, Lee HS, Kang SG (2015) A novel CO-responsive transcriptional regulator and enhanced H2 production by an engineered Thermococcus onnurineus NA1 strain. Appl Environ Microbiol 81:1708–1714

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  128. Shen N, Dai K, Xia X, Jianxiong R, Zhang F (2018) Conversion of syngas (CO and H2) to biochemicals by mixed culture fermentation in mesophilic and thermophilic hollow- fiber membrane biofilm reactors. J Clean Prod 202:536–542

    Article  CAS  Google Scholar 

  129. Shen Y, Brown R, Wen Z (2014) Syngas fermentation of Clostridium carboxidivoran P7 in a hollow fiber membrane biofilm reactor: evaluating the mass transfer coefficient and ethanol production performance. Biochem Eng J 85:21–29

    Article  CAS  Google Scholar 

  130. Kim Y, Lee H (2016) Use of magnetic nanoparticles to enhance bioethanol production in syngas fermentation. Bioresour Technol 204:139–144

    Article  CAS  PubMed  Google Scholar 

  131. Zhu H, Shanks BH, Heindel TJ (2008) Enhancing CO-water mass transfer by functionalized MCM41 nanoparticles. Ind Eng Chem Res 47:7881–7887

    Article  CAS  Google Scholar 

  132. Fang X, Wang Y, Wang Z, Jiang Z, Dong M (2019) Microorganism assisted synthesized nanoparticles for catalytic applications. Energies 12:1–21

    Article  Google Scholar 

  133. Hulkoti NI, Taranath TC (2014) Biosynthesis of nanoparticles using microbes—a review. Colloids Surf B Biointerf 121:474–483

    Article  CAS  Google Scholar 

  134. Pereira L, Mehboob F, Stams AJM, Mota MM, Rijnaarts HHM, Alves MM (2015) Metallic nanoparticles: microbial synthesis and unique properties for biotechnological applications, bioavailability and biotransformation. Crit Rev Biotechnol 35:114–128

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Instituto de Tecnologia Química e Biológica Antonio Xavier, Universidade Nova de Lisboa, ITQB-NOVA, Oeiras, Portugal

    Mónica Martins & Inês A. C. Pereira

  2. Instituto de Catálisis y Petroleoquímica, CSIC, Madrid, Spain

    Marcos Pita & Antonio L. De Lacey

Authors
  1. Mónica Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Inês A. C. Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marcos Pita
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Antonio L. De Lacey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Antonio L. De Lacey .

Editor information

Editors and Affiliations

  1. LAQV, REQUIMTE, NOVA School of Science and Technology, Caparica, Portugal

    José J. G. Moura

  2. LAQV, REQUIMTE, NOVA School of Science and Technology, Caparica, Portugal

    Isabel Moura

  3. LAQV, REQUIMTE, NOVA School of Science and Technology, Caparica, Portugal

    Luisa B. Maia

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Martins, M., Pereira, I.A.C., Pita, M., De Lacey, A.L. (2021). Biological Production of Hydrogen. In: Moura, J.J.G., Moura, I., Maia, L.B. (eds) Enzymes for Solving Humankind's Problems. Springer, Cham. https://doi.org/10.1007/978-3-030-58315-6_9

Download citation

Publish with us

Policies and ethics

Search

Navigation