Photosynthesis Research

, Volume 126, Issue 2–3, pp 237–247 | Cite as

Photobiological hydrogen production and artificial photosynthesis for clean energy: from bio to nanotechnologies

  • K. Nath
  • M. M. Najafpour
  • R. A. Voloshin
  • S. E. Balaghi
  • E. Tyystjärvi
  • R. Timilsina
  • J. J. Eaton-Rye
  • T. Tomo
  • H. G. Nam
  • H. Nishihara
  • S. Ramakrishna
  • J.-R. Shen
  • S. I. AllakhverdievEmail author


Global energy demand is increasing rapidly and due to intensive consumption of different forms of fuels, there are increasing concerns over the reduction in readily available conventional energy resources. Because of the deleterious atmospheric effects of fossil fuels and the uncertainties of future energy supplies, there is a surge of interest to find environmentally friendly alternative energy sources. Hydrogen (H2) has attracted worldwide attention as a secondary energy carrier, since it is the lightest carbon-neutral fuel rich in energy per unit mass and easy to store. Several methods and technologies have been developed for H2 production, but none of them are able to replace the traditional combustion fuel used in automobiles so far. Extensively modified and renovated methods and technologies are required to introduce H2 as an alternative efficient, clean, and cost-effective future fuel. Among several emerging renewable energy technologies, photobiological H2 production by oxygenic photosynthetic microbes such as green algae and cyanobacteria or by artificial photosynthesis has attracted significant interest. In this short review, we summarize the recent progress and challenges in H2-based energy production by means of biological and artificial photosynthesis routes.


Artificial photosynthesis Hydrogen as clean energy Cyanobacteria Light-harvesting complexes Nanotechnology Photobiological hydrogen production 





Carbon dioxide




Oxidized form of ferredoxin


Reduced form of ferredoxin



PS I and PS II

Photosystem I and photosystem II


Light-harvesting complexes


Natural gas reformation reaction


High-temperature thermochemical water splitting


Nuclear high-temperature electrolysis


Normal cubic meter


Transmission electron microscopy


High-resolution transmission electron microscopy


Water-oxidizing complex



MMN is grateful to the Institute for Advanced Studies in Basic Sciences, and the National Elite Foundation for financial support. SEB is grateful to Young Researchers and Elite Club for financial support. ET was supported by Academy of Finland and Nordic Energy Research (Aquafeed project). HGN was supported by Institute for Basic Sciences (IBS-R013-D1-2015-a00), Korea. This work was also supported by a grant-in-aid for Specially Promoted Research No. 24000018 from JSPS, MEXT (Japan) to JRS, and by a grant from the Russian Science Foundation (No: 14-14-00039) to SIA.


  1. Abraham S (2002) Toward a more secure and cleaner energy future for America: national hydrogen energy roadmap; production, delivery, storage, conversion, applications, public education and outreach. US Department Energy, WashingtonGoogle Scholar
  2. Adamson AW, Demas JN (1971) New photosensitizer. Tris (2, 2′-bipyridine) ruthenium (II) chloride. J Am Chem Soc 93:1800–1801CrossRefGoogle Scholar
  3. Allakhverdiev SI (2012) Photosynthetic and biomimetic hydrogen production. Int J Hydrog Energy 37:8744–8752CrossRefGoogle Scholar
  4. Allakhverdiev SI, Kreslavski VD, Thavasi V, Zharmukhamedov SK, Klimov VV, Nagata T, Nishihara H, Ramakrishna S (2009) Hydrogen photoproduction by use of photosynthetic organisms and biomimetic systems. Photochem Photobiol Sci 8:148–156CrossRefPubMedGoogle Scholar
  5. Allakhverdiev SI, Thavasi V, Kreslavski VD, Zharmukhamedov SK, Klimov VV, Ramakrishna S, Los DA, Mimuro M, Nishihara H, Carpentier R (2010a) Photosynthetic hydrogen production. J Photochem Photobiol C 11:87–99CrossRefGoogle Scholar
  6. Allakhverdiev SI, Kreslavski VD, Thavasi V, Zharmukhamedov SK, Klimov VV, Nishihara H, Ramakrishna S, Mimuro M, Carpentier R, Nagata T (2010b) Photosynthetic energy conversion: hydrogen photoproduction by natural and biomimetic systems. In: Mukherjee Amitava (ed) Biomimetics, learning from nature. IN-TECH, Vukovar, pp 49–76Google Scholar
  7. Allen JF (1975) Oxygen reduction and optimum production of ATP in photosynthesis. Nature 256:599–600. doi: 10.1038/256599a0 CrossRefGoogle Scholar
  8. Araújo WL, Nunes-Nesi A, Fernie AR (2014) On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions. Photosynth Res 119:141–156CrossRefPubMedGoogle Scholar
  9. Arnon DI (1959) Conversion of light into chemical energy in photosynthesis. Nature 184:10–20PubMedGoogle Scholar
  10. Azwar MY, Hussain MA, Abdul-Wahab AK (2014) Development of biohydrogen production by photobiological, fermentation and electrochemical processes: a review. Renew Sustain Energy Rev 31:158–173CrossRefGoogle Scholar
  11. Baker NR (2008) Chlorophyll fluorescence: a Probe of Photosynthesis in vivo. Annu Rev Plant Biol 59:89–113CrossRefPubMedGoogle Scholar
  12. Bandyopadhyay A, Stöckel J, Min H et al (2010) High rates of photobiological H2 production by a cyanobacterium under aerobic conditions. Nat Commun 1:139CrossRefPubMedGoogle Scholar
  13. Björkman O, Demmig-Adams B (1995) Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. Ecophysiology photosynthesis. Springer, Berlin, pp 17–47CrossRefGoogle Scholar
  14. Björn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: Why chlorophyll a? Photosynth Res 99:85–98. doi: 10.1007/s11120-008-9395-x CrossRefPubMedGoogle Scholar
  15. Chou LY, Liu R, He W, Geh N, Lin Y, Hou EYF, Wang D, Hou HJM (2012) Direct oxygen and hydrogen production by water splitting using a robust bioinspired manganese-oxo oligomer complex/tungsten oxide catalytic system. Int J Hydrog Energy 37:8889–8896CrossRefGoogle Scholar
  16. Ciamician G (1912) The photochemistry of the future. Science 36:385–394Google Scholar
  17. Concepcion JJ, Jurss JW, Templeton JL, Meyer TJ (2008) Mediator-assisted water oxidation by the ruthenium “blue dimer” cis, cis-[(bpy) 2 (H2O) RuORu (OH2)(bpy) 2] 4+. Proc Natl Acad Sci 105:17632–17635PubMedCentralCrossRefPubMedGoogle Scholar
  18. Eberhard S, Finazzi G, Wollman F-A (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515. doi: 10.1146/annurev.genet.42.110807.091452 CrossRefPubMedGoogle Scholar
  19. Esper B, Badura A, Rögner M (2006) Photosynthesis as a power supply for (bio-) hydrogen production. Trends Plant Sci 11:543–549CrossRefPubMedGoogle Scholar
  20. Ewan BCR, Allen RWK (2005) A figure of merit assessment of the routes to hydrogen. Int J Hydrog Energy 30:809–819CrossRefGoogle Scholar
  21. Ferreira KN, Iverson TM, Maghlaoui K et al (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838CrossRefPubMedGoogle Scholar
  22. Flexas J, Briantais J-M, Cerovic Z et al (2000) Steady-state and maximum chlorophyll fluorescence responses to water stress in grapevine leaves: a new remote sensing system. Remote Sens Environ 73:283–297CrossRefGoogle Scholar
  23. Flexas J, Escalona JM, Evain S et al (2002) Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water-stress in C3 plants. Physiol Plant 114:231–240CrossRefPubMedGoogle Scholar
  24. Freedman A, Cavender-Bares J, Kebabian PL et al (2002) Remote sensing of solar-excited plant fluorescence as a measure of photosynthetic rate. Photosynthetica 40:127–132CrossRefGoogle Scholar
  25. Gaffron H (1939) Reduction of CO2 with H2 in green plants. Nature 143:204–205CrossRefGoogle Scholar
  26. Gafney HD, Adamson AW (1972) Excited state Ru (bipyr) 32 + as an electron-transfer reductant. J Am Chem Soc 94:8238–8239CrossRefGoogle Scholar
  27. Garbulsky MF, Filella I, Verger A, Peñuelas J (2013) Photosynthetic light use efficiency from satellite sensors: From global to Mediterranean vegetation. Environ. Exp, BotGoogle Scholar
  28. Gust D, Moore TA, Moore AL (2009) Solar fuels via artificial photosynthesis. Acc Chem Res 42:1890–1898CrossRefPubMedGoogle Scholar
  29. Hemschemeier A, Melis A, Happe T (2009) Analytical approaches to photobiological hydrogen production in unicellular green algae. Photosynth Res 102:523–540PubMedCentralCrossRefPubMedGoogle Scholar
  30. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230CrossRefGoogle Scholar
  31. Imahori H, Mori Y, Matano Y (2003) Nanostructured artificial photosynthesis. J Photochem Photobiol C 4:51–83CrossRefGoogle Scholar
  32. Iyer A, Del-Pilar J, Kingondu CK et al (2012) Water oxidation catalysis using amorphous manganese oxides, octahedral molecular sieves (OMS-2), and octahedral layered (OL-1) manganese oxide structures. J Phys Chem C 116:6474–6483CrossRefGoogle Scholar
  33. Kotay SM, Das D (2008) Biohydrogen as a renewable energy resource-prospects and potentials. Int J Hydrog Energy 33:258–263CrossRefGoogle Scholar
  34. Limburg J, Vrettos JS, Liable-Sands LM, Rheingold AL, Crabtree RH, Brudvig GW (1999) A functional model for O–O bond formation by the O2-evolving complex in photosystem II. Science 283:1524–1527CrossRefPubMedGoogle Scholar
  35. Lynd LR, Larson E, Greene N et al (2009) The role of biomass in America’s energy future: framing the analysis. Biofuels Bioprod Biorefining 3:113–123CrossRefGoogle Scholar
  36. Maitra U, Lingampalli SR, Rao CNR (2014) Artificial photosynthesis and the splitting of water to generate hydrogen. Curr Sci 106:518–527Google Scholar
  37. Maness P-C, Yu J, Eckert C, Ghirardi ML (2009) Photobiological hydrogen production—prospects and challenges. Microbe Magazine 4(6):275–280Google Scholar
  38. Maurino VG, Weber APM (2013) Engineering photosynthesis in plants and synthetic microorganisms. J Exp Bot. doi: 10.1093/jxb/ers263 PubMedGoogle Scholar
  39. Maxwell K (2000) Chlorophyll fluorescence–a practical guide. J Exp Bot 51:659–668CrossRefPubMedGoogle Scholar
  40. Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748PubMedCentralCrossRefPubMedGoogle Scholar
  41. Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566PubMedCentralCrossRefPubMedGoogle Scholar
  42. Najafpour MM (2011) Hollandite as a functional and structural model for the biological water oxidizing complex: manganese-calcium oxide minerals as a possible evolutionary origin for the camn4 cluster of the biological water oxidizing complex. Geomicrobiol J 28:714–718CrossRefGoogle Scholar
  43. Najafpour MM, Allakhverdiev SI (2012) Manganese compounds as water oxidizing catalysts for hydrogen production via water splitting: from manganese complexes to nano-sized manganese oxides. Int J Hydrog Energy 37:8753–8764CrossRefGoogle Scholar
  44. Najafpour MM, Tabrizi AM, Cecil K (2013) Nano-size layered manganese–calcium oxide as an efficient and biomimetic catalyst for water oxidation under acidic conditions: comparable to platinum. Dalton Trans 42:5085–5091CrossRefPubMedGoogle Scholar
  45. Najafpour MM, Ghobadi MZ, Sedigh DJ, Haghighi B (2014a) Nano-sized layered manganese oxide in a poly-l-glutamic acid matrix: a biomimetic, homogenized, heterogeneous structural model for the water-oxidizing complex in photosystem II. RSC Adv 4:39077–39081CrossRefGoogle Scholar
  46. Najafpour MM, Isaloo MA, Eaton-Rye JJ, Tomo T, Nishihara H, Satoh K, Carpentier R, Shen JR, Allakhverdiev SI (2014b) Water exchange in manganese-based water-oxidizing catalysts in photosynthetic systems: from the water-oxidizing complex in photosystem II to nano-sized manganese oxides. Biochim Biophys Acta 1837(9):1395–1410CrossRefPubMedGoogle Scholar
  47. Nam YS, Magyar AP, Lee D et al (2010) Biologically templated photocatalytic nanostructures for sustained light-driven water oxidation. Nat Nanotechnol 5:340–344CrossRefPubMedGoogle Scholar
  48. Nath K, Elizabeth J, Poudyal RS et al (2013a) Mobilization of photosystem II-light harvesting complex II supercomplexes during high light illumination and state transitions. Rapid Commun Photosci 2:18–23. doi: 10.5857/RCP.2013.2.1.018 CrossRefGoogle Scholar
  49. Nath K, Phee B-K, Jeong S et al (2013b) Age-dependent changes in the functions and compositions of photosynthetic complexes in the thylakoid membranes of Arabidopsis thaliana. Photosynth Res 117:547–556CrossRefPubMedGoogle Scholar
  50. Nocera DG (2012) The artificial leaf. Acc Chem Res 45:767–776CrossRefPubMedGoogle Scholar
  51. Pena MA, Gómez JP, Fierro JLG (1996) New catalytic routes for syngas and hydrogen production. Appl Catal A 144:7–57CrossRefGoogle Scholar
  52. Porcar-Castell A (2011) A high-resolution portrait of the annual dynamics of photochemical and non-photochemical quenching in needles of Pinus sylvestris. Physiol Plant 143:139–153CrossRefPubMedGoogle Scholar
  53. Rascher U, Damm A, van der Linden S et al (2010) Sensing of photosynthetic activity of crops. Precision crop protection challenge use heterogeneity. Springer, Netherlands, pp 87–99CrossRefGoogle Scholar
  54. Rathmann R, Szklo A, Schaeffer R (2010) Land use competition for production of food and liquid biofuels: an analysis of the arguments in the current debate. Renew Energy 35:14–22CrossRefGoogle Scholar
  55. Rathmann R, Szklo A, Schaeffer R (2012) Targets and results of the Brazilian biodiesel incentive program-has it reached the promised land? Appl Energy 97:91–100CrossRefGoogle Scholar
  56. Rey FE, Heiniger EK, Harwood CS (2007) Redirection of metabolism for biological hydrogen production. Appl Environ Microbiol 73:1665–1671PubMedCentralCrossRefPubMedGoogle Scholar
  57. Rostrup-Nielsen JR (1984) Sulfur-passivated nickel catalysts for carbon-free steam reforming of methane. J Catal 85:31–43CrossRefGoogle Scholar
  58. Schütz K, Happe T, Troshina O et al (2004) Cyanobacterial H2 production-a comparative analysis. Planta 218:350–359CrossRefPubMedGoogle Scholar
  59. Searchinger T, Heimlich R, Houghton RA et al (2008) Use of US croplands for biofuels increases greenhouse gases through emissions from land-use change. Science 319:1238–1240CrossRefPubMedGoogle Scholar
  60. Soukupová J, Cséfalvay L, Urban O et al (2008) Annual variation of the steady-state chlorophyll fluorescence emission of evergreen plants in temperate zone. Funct Plant Biol 35:63–76CrossRefGoogle Scholar
  61. Suga M, Akita F, Hirata K et al (2015) Native structure of photosystem II at 1.95 A resolution viewed by femtosecond X-ray pulses. Nature 517:99–103Google Scholar
  62. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60CrossRefPubMedGoogle Scholar
  63. Whitmarsh J (1999) The photosynthetic process. Concepts photobiology. Springer, Netherlands, pp 11–51CrossRefGoogle Scholar
  64. Williams CR, Bees MA (2014) Mechanistic modeling of sulfur-deprived photosynthesis and hydrogen production in suspensions of chlamydomonas reinhardtii. Biotechnol Bioeng 111:320–335Google Scholar
  65. Zarco-Tejada PJ, Pushnik JC, Dobrowski S, Ustin SL (2003) Steady-state chlorophyll a fluorescence detection from canopy derivative reflectance and double-peak red-edge effects. Remote Sens Environ 84:283–294CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • K. Nath
    • 1
    • 2
  • M. M. Najafpour
    • 3
    • 4
  • R. A. Voloshin
    • 5
  • S. E. Balaghi
    • 6
  • E. Tyystjärvi
    • 7
  • R. Timilsina
    • 8
  • J. J. Eaton-Rye
    • 9
  • T. Tomo
    • 10
    • 11
  • H. G. Nam
    • 8
  • H. Nishihara
    • 12
  • S. Ramakrishna
    • 13
  • J.-R. Shen
    • 14
  • S. I. Allakhverdiev
    • 5
    • 15
    • 16
    Email author
  1. 1.Research Institute for Next Generation (RING)KathmanduNepal
  2. 2.Department of Biological SciencesWestern Michigan UniversityKalamazooUSA
  3. 3.Department of ChemistryInstitute for Advanced Studies in Basic Sciences (IASBS)ZanjanIran
  4. 4.Center of Climate Change and Global WarmingInstitute for Advanced Studies in Basic Sciences (IASBS)ZanjanIran
  5. 5.Controlled Photobiosynthesis Laboratory, Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  6. 6.Young Researchers and Elite Club, Shiraz BranchIslamic Azad UniversityShirazIran
  7. 7.Department of Biochemistry / Molecular Plant BiologyUniversity of TurkuTurkuFinland
  8. 8.Center for Plant Aging Research, Institute for Basic Science, and Department of New BiologyDGISTDaeguRepublic of Korea
  9. 9.Department of BiochemistryUniversity of OtagoDunedinNew Zealand
  10. 10.Department of Biology, Faculty of ScienceTokyo University of ScienceTokyoJapan
  11. 11.PRESTOJapan Science and Technology Agency (JST)SaitamaJapan
  12. 12.Department of Chemistry, School of ScienceThe University of TokyoTokyoJapan
  13. 13.Department of Mechanical Engineering, Center for Nanofibers and NanotechnologyNational University of SingaporeSingaporeSingapore
  14. 14.Photosynthesis Research Center, Graduate School of Natural Science and Technology, Faculty of ScienceOkayama UniversityOkayamaJapan
  15. 15.Institute of Basic Biological ProblemsRussian Academy of SciencesPushchinoRussia
  16. 16.Department of Plant Physiology, Faculty of BiologyM.V. Lomonosov Moscow State UniversityMoscowRussia

Personalised recommendations