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Integrating dark and light bio-hydrogen production strategies: towards the hydrogen economy

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Abstract

Biological methods of hydrogen production are preferable to chemical methods because of the possibility to use sunlight, CO2 and organic wastes as substrates for environmentally benign conversions, under moderate conditions. By combining different microorganisms with different capabilities, the individual strengths of each may be exploited and their weaknesses overcome. Mechanisms of bio-hydrogen production are described and strategies for their integration are discussed. Dual systems can be divided broadly into wholly light-driven systems (with microalgae/cyanobacteria as the 1st stage) and partially light-driven systems (with a dark, fermentative initial reaction). Review and evaluation of published data suggests that the latter type of system holds greater promise for industrial application. This is because the calculated land area required for a wholly light-driven dual system would be too large for either centralised (macro-) or decentralised (micro-) energy generation. The potential contribution to the hydrogen economy of partially light-driven dual systems is overviewed alongside that of other bio-fuels such as bio-methane and bio-ethanol.

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Abbreviations

ADP:

Adenosine diphosphate

Akinete:

Vegetative cyanobacterial cell accumulating carbohydrate. The main component of filaments, including heterocysts

APB:

Anoxygenic photosynthetic bacteria

ATP:

Adenosine triphosphate

Autotrophy:

Metabolism with the synthesis of carbohydrate using light and/or inorganic substrates

Av.:

Average

Axenic:

Pure culture containing only one type of microorganism

BOD:

Biological oxygen demand the mass of oxygen consumed by microorganisms during the oxidation of organic compounds from a sample of water

COD:

Chemical oxygen demand the mass of oxygen consumed during the chemical oxidation of organic compounds from a sample of water

CSTR:

Continuous stirred tank reactor

Direct bio-photolysis:

H2 production from water electrons liberated from H2O by photosystem II recombine with H+ to form H2, catalysed by hydrogenase or nitrogenase

DF:

Dark fermentation

DF–PF:

Dual system combining dark fermentation and photofermentation

DMFC:

Direct methanol fuel cell, a type of PEM-FC using methanol fuel directly without reforming

dw:

Dry cell weight

FHL:

Formate: hydrogen lyase

Fermentation:

Microbial growth mode in which ATP is generated only by substrate level phosphorylation in the absence of exogenous electron acceptors (e.g. O2, NO3 −, NO2 2−, SO4 2−)

HRT:

Hydraulic retention time. The total flow rate though a diluted system over its volume

Indirect bio-photolysis:

H2 production from water via the photosynthesis and fermentation of carbohydrates

Heterocyst:

A cyanobacterial cell specialised for N2 fixation

Heterotrophy:

Microbial metabolism utilising organic carbon sources

HHV:

Higher heating value

Hyperthermophilic:

Refers to extreme thermophiles most active in the temperature range 80–110°C

LDH:

Fermentative lactate dehydrogenase

Light conversion efficiency:

The percentage of available light energy converted to H2, distinct from photosynthetic efficiency (PE)

Mesophilic:

Most active in the temperature range 20–40°C

NADH:

Nicotinamide-adenine dinucleotide

Net energy ratio:

The dimensionless ratio of the energy outputs to primary inputs for the entire operational lifetime of a system

Nitrogenase:

Nitrogenase complex (reductase and nitrogenase)

PE:

Photosynthetic efficiency. The percentage of photosynthetically active light energy converted to H2 (includes only those wavelengths which interact with photopigments)

PEM-FC:

Proton exchange membrane fuel cell a type of low-temperature fuel cell considered most suitable for transport applications

PF:

Photofermentation

PHB:

Poly-β-hydroxybutyrate, a storage polymer

Photoheterotrophy:

Light-driven mode of anaerobic metabolism using organic substrates as electron donors

Pi:

Inorganic phosphate

PFL:

Pyruvate: formate lyase

PFOR:

Pyruvate: ferredoxin oxidoreductase

Photopigments:

Light harvesting proteins

Phototrophy:

Microbial metabolism using light energy

Photoautotrophy:

Microbial metabolism using light energy for the synthesis of carbon sources

PNS bacteria:

Purple non-sulfur bacteria

PSI:

Photosystem I

PSII:

Photosystem II

Reserve:

The amount of a resource in place (e.g. oil in the ground) that is economically recoverable

SOFC:

Solid oxide fuel cell, a high temperature alkaline fuel cell

SOT medium:

Growth medium for cyanobacteria containing salts and trace elements but no carbon source

Thermophilic:

Most active in the temperature range 40–60°C

UASB:

Upstream anaerobic sludge blanket reactor

References

  • Abdullah AZ, Razali N, Mootabadi H, Salamatinia B (2007) Critical technical areas for future improvements in biodiesel technologies. Environ Res Lett 2:034001. doi:10.1088/1748-9326/2/3/034001

    Google Scholar 

  • Akano T, Miura Y, Fukatsu K, Miyasaka H, Ikuta Y, Matsumoto H, Hamasaki A, Shioji N, Mizoguchi T, Yagi K, Maeda I (1996) Hydrogen production by photosynthetic microorganisms. Appl Biochem Biotechnol 57–58:677–688. doi:10.1007/BF02941750

    Google Scholar 

  • Akkerman I, Janssen M, Rocha J, Wijffels RH (2002) Photobiological hydrogen production: photochemical efficiency and bioreactor design. Int J Hydrogen Energy 27(11–12):1195–1208. doi:10.1016/S0360-3199(02)00071-X

    CAS  Google Scholar 

  • Alam KY, Clark DP (1989) Anaerobic fermentation balance of Escherichia coli as observed by in vivo nuclear magnetic resonance spectroscopy. J Bacteriol 171(11):6213–6217

    CAS  Google Scholar 

  • Aldhous P (2006) Green gold. New Sci 25(2540):37–39

    Google Scholar 

  • Anon (2004) United Kingdom food and drink processing mass balance: biffaward programme on sustainable resource use. C-Tech Innovation, Capenhurst

  • Anon (2005) Agriculture in the United Kingdom. Retrieved Aug 2007, from statistics.defra.gov.uk/esg/publications/auk/2005/default.asp

  • Antal TK, Lindblad P (2005) Production of H2 by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. J Appl Microbiol 98(1):114–120. doi:10.1111/j.1365-2672.2004.02431.x

    CAS  Google Scholar 

  • Aoyama K, Uemura I, Miyake J, Asada Y (1997) Photosynthetic bacterial hydrogen production with fermentation products of cyanobacterium Spirulina platensis. International conference on biological hydrogen production, Plenum, New York

  • Asada Y, Tokumoto M, Aihara Y, Oku M, Ishimi K, Wakayama T, Miyake J, Tomiyama M, Kohno H (2006) Hydrogen production by co-cultures of Lactobacillus and a photosynthetic bacterium, Rhodobacter sphaeroides RV. Int J Hydrogen Energy 31(11):1509–1513. doi:10.1016/j.ijhydene.2006.06.017

    CAS  Google Scholar 

  • Avi S (2007) Photovoltaics literature survey (No. 51). Prog Photovolt Res Appl 15(1):87–91. doi:10.1002/pip.747

    Google Scholar 

  • Bae J-H, Bardiya N, Reddy MRVP (2005) Bio-hydrogen: technology and future prospects. In: Lal B, Reddy MRVP (eds) Wealth from waste: trends, technologies. TERI, New Delhi, pp 87–132

    Google Scholar 

  • Banik RM, Santhiagu A, Kanari B, Sabarinath C, Upadhyay SN (2003) Technological aspects of extractive fermentation using aqueous two-phase systems. World J Microbiol Biotechnol 19(4):337–348. doi:10.1023/A:1023940809095

    CAS  Google Scholar 

  • Bartelings H, van Beukering P, Kuik O, Linderhof V, Oosterhuis F, Brander L, Wagtendonk A (2005) Effectiveness of landfill taxation, report prepared for the Dutch Ministry of Housing, spatial planning and the environment, Institute for Environmental Studies, Vrije Universiteit, R-05/05, Amsterdam. Available at www.ivm.falw.vu.nl/research_output/index.cfm/home_subsection.cfm/subsectionid/FF91BCBD-EAFE-426A-ABB8184073A39BBF

  • Basak N, Das D (2007) The prospect of purple non-sulfur (PNS) photosynthetic bacteria for hydrogen production: the present state of the art. World J Microbiol Biotechnol 23:31–42. doi:10.1007/s11274-006-9190-9

    CAS  Google Scholar 

  • Benemann JR (1996) Hydrogen biotechnology: progress and prospects. Nat Biotechnol 14:1101–1103. doi:10.1038/nbt0996-1101

    CAS  Google Scholar 

  • Bevan A, Book D, Züttel A, Harris R (2007) The protium project: a hybrid electric canal boat using metal hydride store and a PEM fuel cell. The Oxford-Kobe energy seminar, 22–24th April. Hydrogen storage: the international grand challenge, Kobe Institute, Japan

  • Biebl H, Pfennig N (1981) Isolation of members of the family Rhodospirillacae. In: Starr MP, Stolp H, Truper HG, Balows A, Schlegel HG (eds) The prokaryotes, vol 1. Springer, Dordrecht, pp 267–273

    Google Scholar 

  • Blankenship RE, Madigan MT, Bauer CE (1995) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht

    Google Scholar 

  • Bock A, Sawers G (1996) Fermentation. In: Niedhardt FC et al (eds) Escherichia coli and Salmonella typhimurium cellular and molecular biology, vol 1. ASM, Washington DC, pp 262–282

    Google Scholar 

  • Borodin VB, Tsygankov AA, Rao KK, Hall DO (2000) Hydrogen production by Anabaena variabilis PK84 under simulated outdoor conditions. Biotechnol Bioeng 69(5):478–485. doi:10.1002/1097-0290(20000905)69:5<478::AID-BIT2>3.0.CO;2-L

    CAS  Google Scholar 

  • Burgess G, Fernandez-Velasco JG (2007) Materials, operational energy inputs, and net energy ratio for photobiological hydrogen production. Int J Hydrogen Energy 32:1225–1234. doi:10.1016/j.ijhydene.2006.10.055

    CAS  Google Scholar 

  • Carrieri D, Ananyev G, Garcia Costas AM, Bryant DA, Dismukes GC (2008) Renewable hydrogen production by cyanobacteria: nickel requirements for optimal hydrogenase activity. Int J Hydrogen Energy 33(8):2014–2022. doi:10.1016/j.ijhydene.2008.02.022

    CAS  Google Scholar 

  • Castenholz RW (1995) Ecology of thermophilic anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 87–103

    Google Scholar 

  • Chandel AK, Chan ES, Rudravaram R, Narusu ML, Rao LV, Ravindra P (2007) Economics and environmental impact of bioethanol production technologies: an appraisal. Biotechnol Mol Biol Rev 2(1):14–32

    Google Scholar 

  • Chen X, Sun Y, Xiu Z, Li X, Zhang D (2006) Stoichiometric analysis of biological hydrogen production by fermentative bacteria. Int J Hydrogen Energy 31:539–549. doi:10.1016/j.ijhydene.2005.03.013

    CAS  Google Scholar 

  • Claassen PAM, de Vrije GJ (2007) Hydrogen from biomass. Public report, BWP II project, Agrotechnology and Food Sciences Group, Wageningen

  • Claassen PAM, van Lier JB, Lopez-Contreras AM, van Niel EWJ, Sijtsma L, Stams AJM, de Vries SS, Weusthuis RA (1999) Utilisation of biomass for the supply of energy carriers. Appl Microbiol Biotechnol 52:741–755. doi:10.1007/s002530051586

    CAS  Google Scholar 

  • Claassen PAM, Budde MAW, Van Noorden GE, Hoekema S, Hazewinkel JHO, Van Groenestijn JW, De Vrije GJ (2004) Biological hydrogen production from agro-food by-products. Total food: exploiting co-products—minimizing waste. Institute of Food Research, Norwich

    Google Scholar 

  • Clark DP (1989) The fermentation pathways of Escherichia coli. FEMS Microbiol Rev 5(3):223–234. doi:10.1016/0168-6445(89)90033-8

    CAS  Google Scholar 

  • Collet C, Adler N, Schwitzguebel J-P, Peringer P (2004) Hydrogen production by Clostridium thermolactum during continuous fermentation of lactose. Int J Hydrogen Energy 29:1479–1485. doi:10.1016/j.ijhydene.2004.02.009

    CAS  Google Scholar 

  • Cornet JF, Favier L, Dussap CG (2003) Modeling stability of photoheterotrophic continuous cultures in photobioreactors. Biotechnol Prog 19:1216–1227. doi:10.1021/bp034041l

    CAS  Google Scholar 

  • Cournac L, Guedeney G, Peltier G, Vignais PM (2004) Sustained photo evolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex. J Bacteriol 186:1737–1746. doi:10.1128/JB.186.6.1737-1746.2003

    CAS  Google Scholar 

  • Dalton H (2005) The Leeuwenhoek lecture 2000 The natural and unnatural history of methane-oxidizing bacteria. Philos Trans R Soc Lond B Biol Sci 360(1458):1207–1222. doi:10.1098/rstb.2005.1657

    CAS  Google Scholar 

  • Das D, Veziroglu TN (2001) Hydrogen production by biological processes: a survey of literature. Int J Hydrogen Energy 26:13–28. doi:10.1016/S0360-3199(00)00058-6

    CAS  Google Scholar 

  • Davila-Vazquez G, Arriaga S, Alatriste-Mondragón F, de León-Rodríguez A, Rosales-Colunga LM, Razo-Flores E (2008a) Fermentative biohydrogen production: trends and perspectives. Rev Environ Sci Biotechnol 7(1):27–45. doi:10.1007/s11157-007-9122-7

    CAS  Google Scholar 

  • Davila-Vazquez G, Alatriste-Mondragón F, de León Rodríguez A, Razo-Flores E (2008b) Fermentative hydrogen production in batch experiments using lactose, cheese whey and glucose: influence of initial substrate concentration and pH. Int J Hydrogen Energy 33(19):4989–4997. doi:10.1016/j.ijhydene.2008.06.065

    CAS  Google Scholar 

  • Dawson L, Boopathy R (2007) Use of post-harvest sugarcane residue for ethanol production. Bioresour Technol 98(9):1695–1699. doi:10.1016/j.biortech.2006.07.029

    CAS  Google Scholar 

  • de Vrije T, Claassen PAM (2003) Dark hydrogen fermentations. In: Reith JH, Wijffels RH, Barten H (eds) Bio-methane & bio-hydrogen. Dutch Biological Hydrogen Foundation, Petten, pp 103–123

    Google Scholar 

  • de Vrije T, Mars AE, Budde MAW, Lai MH, Dijkema C, de Waard P, Claassen PAM (2007) Glycolytic pathway and hydrogen yield studies of the extreme thermophile Caldicellulosiruptor saccharolyticus. Appl Microbiol Biotechnol 74:1358–1367. doi:10.1007/s00253-006-0783-x

    CAS  Google Scholar 

  • Dien BS, Nichols NN, O’Bryan PJ, Bothast RJ (2000) Development of new ethanologenic Escherichia coli strains for fermentation of lignocellulosic biomass. Appl Biochem Biotechnol 84–86:181–196. doi:10.1385/ABAB:84-86:1-9:181

    Google Scholar 

  • Dutta D, De D, Chaudhuri S, Bhattacharya SK (2005) Hydrogen production by cyanobacteria. Microb Cell Fact 4:36. doi:10.1186/1475-2859-4-36

    Google Scholar 

  • Easterly JL, Burnham M (1996) Overview of biomass and waste fuel resources for power production. Biomass Bioenergy 10(2–3):79–92. doi:10.1016/0961-9534(95)00063-1

    CAS  Google Scholar 

  • Eiteman MA, Altman E (2006) Overcoming acetate in Escherichia coli recombinant protein fermentations. Trends Biotechnol 24(11):530–536. doi:10.1016/j.tibtech.2006.09.001

    CAS  Google Scholar 

  • Emanuelsson EAC, Arcangeli JP, Livingston AG (2003) The anoxic extractive membrane bioreactor. Water Res 37(6):1231–1238. doi:10.1016/S0043-1354(02)00487-6

    CAS  Google Scholar 

  • Ensign JC (1977) Biomass production from animal wastes. In: Schlegel HG, Barnea J (eds) Microbial energy conversion. Pergamon, Oxford, pp 455–483

    Google Scholar 

  • Eroğlu I, Aslan K, Gündüz U, Yücel M, Türker L (1997) Continuous hydrogen production by R. sphaeroides O.U. 001. International conference on biological hydrogen production, Plenum, New York

  • Eroğlu E, Gündüz U, Yücel M, Türker L, Eroğlu I (2004) Photobiological hydrogen production by using olive mill wastewater as a sole substrate source. Int J Hydrogen Energy 29:163–171. doi:10.1016/S0360-3199(03)00110-1

    Google Scholar 

  • Eroğlu E, Eroğlu I, Gündüz U, Türker L, Yücel M (2006) Biological hydrogen production from olive mill wastewater with two-stage processes. Int J Hydrogen Energy 31(11):1527–1535. doi:10.1016/j.ijhydene.2006.06.020

    Google Scholar 

  • Eroğlu I, Tabanoğlu A, Gündüz U, Eroğlu E, Yücel M (2008) Hydrogen production by Rhodobacter sphaeroides O.U.001 in a flat plate solar bioreactor. Int J Hydrogen Energy 33:531–541. doi:10.1016/j.ijhydene.2007.09.025

    Google Scholar 

  • Fang HHP, Liu H, Zhang T (2005) Phototrophic hydrogen production from acetate and butyrate in wastewater. Int J Hydrogen Energy 30:785–793. doi:10.1016/j.ijhydene.2004.12.010

    CAS  Google Scholar 

  • Fang HHP, Li C, Zhang T (2006) Acidophilic biohydrogen production from rice slurry. Int J Hydrogen Energy 31:683–692. doi:10.1016/j.ijhydene.2005.07.005

    CAS  Google Scholar 

  • Fascetti E, D’Addario E, Todini O, Robertiello A (1998) Photosynthetic hydrogen evolution with volatile organic acids derived from the fermentation of source selected municipal solid wastes. Int J Hydrogen Energy 23(9):753–760. doi:10.1016/S0360-3199(97)00123-7

    CAS  Google Scholar 

  • Ferchichi M, Crabbe E, Hintz W, Gil GH, Almadidy A (2005) Influence of culture parameters on biological hydrogen production by Clostridium saccharoperbutylacetonicum ATCC 27021. World J Microbiol Biotechnol 21(6–7):855–862. doi:10.1007/s11274-004-5972-0

    CAS  Google Scholar 

  • Filatova LV, Berg IA, Krasil’nikova EN, Tsygankov AA, Laurinavichene TV, Ivanovskii RN (2005a) A study of the mechanism of acetate assimilation in purple nonsulfur bacteria lacking the glyoxylate shunt: acetate assimilation in Rhodobacter sphaeroides. Microbiology 74(3):265–269. doi:10.1007/s11021-005-0061-4

    CAS  Google Scholar 

  • Filatova LV, Berg IA, Krasil’nikova EN, Ivanovskii RN (2005b) A study of the mechanism of acetate assimilation in purple nonsulfur bacteria lacking the glyoxylate shunt: enzymes of the citramalate cycle in Rhodobacter sphaeroides. Microbiology 74(3):270–278. doi:10.1007/s11021-005-0062-3

    CAS  Google Scholar 

  • Filho PA, Badr O (2004) Biomass resources for energy in north-eastern Brazil. Appl Energy 77:51–67. doi:10.1016/S0306-2619(03)00095-3

    Google Scholar 

  • Fissler J, Kohring GW, Giffhorn F (1995) Enhanced hydrogen production from aromatic acids by immobilized cells of Rhodopseudomonas palustris. Appl Microbiol Biotechnol 44:43–46. doi:10.1007/BF00164478

    CAS  Google Scholar 

  • Franchi E, Tosi C, Scolla G, Penna GD, Rodriguez F, Pedroni PM (2004) Metabolically engineered Rhodobacter sphaeroides RV strains for improved biohydrogen photoproduction combined with disposal of food wastes. Mar Biotechnol 6:552–565. doi:10.1007/s10126-004-1007-y

    CAS  Google Scholar 

  • Fuji T, Tarusawa M, Miyanaga M, Kiyota S, Watanabe T, Yabuki M (1987) Hydrogen production from alcohols, malate and mixed electron donors by Rhodopseudomonas sp. No. 7. Agric Biol Chem 51(1):1–7

    Google Scholar 

  • Ghirardi ML, King PW, Posewitz MC, Maness PC, Fedorov A, Kim K, Cohen J, Schulten K, Seibert M (2005) Approaches to developing biological H2-photoproducing organisms and processes. Biochem Soc Trans 33:70–72. doi:10.1042/BST0330070

    CAS  Google Scholar 

  • Goldemberg J (2007) Ethanol for a sustainable energy future. Science 315:808–810. doi:10.1126/science.1137013

    CAS  Google Scholar 

  • Gosse JL, Engel BJ, Rey FE, Harwood CS, Scriven LE, Flickinger MC (2007) Hydrogen production by photoreactive nanoporous latex coatings of nongrowing Rhodopseudomonas palustris CGA009. Biotechnol Prog 23(1):124–130. doi:10.1021/bp060254+

    CAS  Google Scholar 

  • Grosse S, Laramee L, Wendlandt K-D, McDonald IR, Miguez CB, Kleber H-P (1999) Purification and characterization of the soluble methane monooxygenase of the type II methanotrophic nacterium Methylocystis sp. strain WI 14. Appl Environ Microbiol 65(9):3929–3935

    CAS  Google Scholar 

  • Gübitz GM, Mittelbach M, Trabi M (1999) Exploitation of the tropical oil seed plant Jatropha curcas L. Bioresour Technol 67:73–82. doi:10.1016/S0960-8524(99)00069-3

    Google Scholar 

  • Hallenbeck PC (2005) Fundamentals of the fermentative production of hydrogen. Water Sci Technol 52(1–2):21–29

    CAS  Google Scholar 

  • Hallenbeck PC, Benemann JR (2002) Biological hydrogen production; fundamentals and limiting processes. Int J Hydrogen Energy 27(11–12):1185–1193. doi:10.1016/S0360-3199(02)00131-3

    CAS  Google Scholar 

  • Happe T, Schutz K, Bohme H (2000) Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 182(6):1624–1631. doi:10.1128/JB.182.6.1624-1631.2000

    CAS  Google Scholar 

  • Haq Z, Easterly JL (2006) Agricultural residue availability in the United States. Appl Biochem Biotechnol 129–132:3–21. doi:10.1385/ABAB:129:1:3

    Google Scholar 

  • Hassan MA, Shirai Y, Kusubayashi N, Karim MIA, Nakanishi K, Hashimoto K (1997) The production of polyhydroxyalkanoate from anaerobically treated palm oil mill effluent by Rhodobacter sphaeroides. J Ferment Bioeng 83(5):485–488. doi:10.1016/S0922-338X(97)83007-3

    CAS  Google Scholar 

  • Hawkes FR, Dinsdale R, Hawkes DL, Hussy I (2002) Sustainable fermentative hydrogen production: challenges for process optimisation. Int J Hydrogen Energy 27:1339–1347. doi:10.1016/S0360-3199(02)00090-3

    CAS  Google Scholar 

  • Hawkes FR, Hussy I, Kyazze G, Dinsdale R, Hawkes DL (2007) Continuous dark fermentative hydrogen production by mesophilic microflora: principles and progress. Int J Hydrogen Energy 32:172–184. doi:10.1016/j.ijhydene.2006.08.014

    CAS  Google Scholar 

  • Hawkes FR, Forsey H, Premier GC, Dinsdale RM, Hawkes DL, Guwy AJ, Maddy J, Cherryman S, Shine J, Auty D (2008) Fermentative production of hydrogen from a wheat flour industry co-product. Bioresour Technol 99:5020–5029. doi:10.1016/j.biortech.2007.09.010

    CAS  Google Scholar 

  • Hill J, Nelson E, Tilman D, Polasky S, Tiffany D (2006) Environmental, economic, and energetic costs and benefits of biodiesel and ethanol biofuels. Proc Natl Acad Sci USA 103:11206–11210. doi:10.1073/pnas.0604600103

    CAS  Google Scholar 

  • Hillmer P, Gest H (1977a) H2 metabolism in the photosynthetic bacterium Rhodopseudomonas capsulata: H2 production by growing cultures. J Bacteriol 129(2):724–731

    CAS  Google Scholar 

  • Hillmer P, Gest H (1977b) H2 metabolism in the photosynthetic bacterium Rhodopseudomonas capsulata: production and utilisation of H2 by resting cells. J Bacteriol 129(2):732–739

    CAS  Google Scholar 

  • Hoekema S, Bijmans M, Janssen M, Tramper J, Wijffels RH (2002) A pneumatically agitated flat-panel photobioreactor with gas re-circulation: anaerobic photoheterotrophic cultivation of a purple non-sulfur bacterium. Int J Hydrogen Energy 27(11–12):1331–1338. doi:10.1016/S0360-3199(02)00106-4

    CAS  Google Scholar 

  • Hoekema S, Douma RD, Janssen M, Tramper J, Wijffels RH (2006) Controlling light-use by Rhodobacter capsulatus continuous cultures in a flat-panel photobioreactor. Biotechnol Bioeng 95(4):613–626. doi:10.1002/bit.20907

    CAS  Google Scholar 

  • Holmes B, Jones N (2003) Brace yourself for the end of cheap oil. New Sci 179(2406):9

    Google Scholar 

  • Hustede E, Steinbuchel A, Schlegel HG (1993) Relationship between the photoproduction of hydrogen and the accumulation of PHB in nonsulfur purple bacteria. Appl Microbiol Biotechnol 39(1):87–93

    CAS  Google Scholar 

  • Ike A, Toda N, Murakawa T, Hirata K, Miyamoto K (1997) Hydrogen photoproduction from starch in CO2-fixing microalgal biomass by a halotolerant bacterial community. In: Zaborsky OR (ed) Biohydrogen. Hawaii, Plenum, New York and London, pp 311–318

    Google Scholar 

  • Ike A, Kawaguchi H, Hirata K, Miyamoto K (2001) Hydrogen photoproduction from starch in algal biomass. In: Miyake J, Matsunaga T, San Pietro A (eds) Biohydrogen II: an approach to environmentally acceptable technology. Pergamon, Oxford, pp 53–61

    Google Scholar 

  • Ikuta Y, Akano T, Shioji N, Maeda I (1997) Hydrogen production by photosynthetic microorganisms. In: Zaborsky OR (ed) Biohydrogen. Hawaii, Plenum, New York and London, pp 319–327

  • Ivanovskii RN, Krasil’nikova EN, Berg IA (1997) The mechanism of acetate assimilation in the purple nonsulfur bacterium Rhodospirillum rubrum lacking isocitrate lyase. Microbiology 66(6):621–626

    CAS  Google Scholar 

  • Jahn A, Keuntje B, Dorffler M, Klipp W, Oelze J (1994) Optimizing photoheterotrophic H2 production by Rhodobacter capsulatus upon interposon mutagenesis in the hupL gene. Appl Microbiol Biotechnol 40:687–690. doi:10.1007/BF00173330

    CAS  Google Scholar 

  • Jo JH, Lee DS, Park JM (2006) Modeling and optimization of photosynthetic hydrogen gas production by green alga Chlamydomonas reinhardtii in sulfur-deprived circumstance. Biotechnol Prog 22(2):431–437. doi:10.1021/bp050258z

    CAS  Google Scholar 

  • Kadar Z, de Vrije T, van Noorden GE, Budde MAW, Szengyel Z, Reczey K, Claassen PAM (2004) Yields from glucose, xylose, and paper sludge hydrolysate during hydrogen production by the extreme thermophile Caldicellulosiruptor saccharolyticus. Appl Biochem Biotechnol 113–116:497–508. doi:10.1385/ABAB:114:1-3:497

    Google Scholar 

  • Karlsson A, Vallin L, Ejlertsson J (2008) Effects of temperature, hydraulic retention time and hydrogen extraction rate on hydrogen production from the fermentation of food industry residues and manure. Int J Hydrogen Energy 33(3):953–962. doi:10.1016/j.ijhydene.2007.10.055

    CAS  Google Scholar 

  • Kataoka N, Miya A, Kiriyama K (1997) Studies on hydrogen production by continuous culture system of hydrogen-producing anaerobic bacteria. Water Sci Technol 36(6–7):41–47. doi:10.1016/S0273-1223(97)00505-2

    CAS  Google Scholar 

  • Katsuda T, Arimoto T, Igarashi K, Azuma M, Kato J, Takakuwa S, Ooshima H (2000) Light intensity distribution in the externally illuminated cylindrical photo-bioreactor and it’s application to hydrogen production by Rhodobacter capsulatus. Biochem Eng J 5:157–164. doi:10.1016/S1369-703X(00)00054-1

    CAS  Google Scholar 

  • Kawaguchi H, Hashimoto K, Hirata K, Miyamoto K (2001) H2 production from algal biomass by a mixed culture of Rhodobium marinum A-501 and Lactobacillus amylovorus. J Biosci Bioeng 91(3):277–282. doi:10.1263/jbb.91.277

    CAS  Google Scholar 

  • Keeling CD, Whorf TP (2005) Atmospheric CO2 records from sites in the SIO air sampling network. Trends: a compendium of data on global change. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak Ridge

  • Kern M, Koch HG, Klemme JH (1992) EDTA activation of H2 photoproduction by Rhodospirillum rubrum. Appl Microbiol Biotechnol 37(4):496–500. doi:10.1007/BF00180976

    CAS  Google Scholar 

  • Khatipov E, Miyake M, Miyake J, Asada Y (1998) Accumulation of poly--hydroxybutyrate by Rhodobacter sphaeroides on various carbon and nitrogen substrates. FEMS Microbiol Lett 162:39–45

    CAS  Google Scholar 

  • Kim M-S, Lee TJ, Yoon YS, Lee IG, Moon KW (2001) Hydrogen production from food processing wastewater and sewage sludge by anaerobic dark fermentation combined with photo-fermentation. In: Miyake J, Matsunaga T, San Pietro A (eds) Biohydrogen II: an approach to environmentally acceptable technology. Pergamon, Oxford, pp 263–272

    Google Scholar 

  • Kim NJ, Lee JK, Lee CJ (2004a) Pigment reduction to improve photosynthetic productivity of Rhodobacter sphaeroides. J Gen Microbiol 1692(28):607–616

    Google Scholar 

  • Kim S-H, Han S-K, Shin H-S (2004b) Feasibility of biohydrogen production by anaerobic co-digestion of food waste and sewage sludge. Int J Hydrogen Energy 29:1607–1616. doi:10.1016/j.ijhydene.2004.02.018

    CAS  Google Scholar 

  • Kim E-J, Kim J-S, Kim M-S, Lee JK (2006a) Effect of changes in the level of light harvesting complexes of Rhodobacter sphaeroides on the photoheterotrophic production of hydrogen. Int J Hydrogen Energy 31:531–538. doi:10.1016/j.ijhydene.2005.04.053

    CAS  Google Scholar 

  • Kim M-S, Baek J-S, Lee JK (2006b) Comparison of H2 accumulation by Rhodobacter sphaeroides KD131 and its uptake hydrogenase and PHB synthase deficient mutant. Int J Hydrogen Energy 31:121–127. doi:10.1016/j.ijhydene.2004.10.023

    CAS  Google Scholar 

  • Kim M-S, Baek J-S, Yun Y-S, Sim SJ, Park S, Kim S-C (2006c) Hydrogen production from Chlamydomonas reinhardtii biomass using a two-step conversion process: anaerobic conversion and photosynthetic fermentation. Int J Hydrogen Energy 31:812–816. doi:10.1016/j.ijhydene.2005.06.009

    CAS  Google Scholar 

  • Kirkpatrick C, Maurer LM, Oyelakin NE, Yoncheva YN, Maurer R, Slonczewski JL (2001) Acetate and formate stress: opposite responses in the proteome of Escherichia coli. J Bacteriol 183(21):6466–6477. doi:10.1128/JB.183.21.6466-6477.2001

    CAS  Google Scholar 

  • Knappe J (1987) Anaerobic dissimilation of pyruvate. In: Niedhardt FC (ed) Escherichia coli and Salmonella typhimurium, vol 1. American Society for Microbiology, Washington DC, pp 151–155

    Google Scholar 

  • Ko IB, Noike T (2002) Use of blue optical filters for suppression of growth of algae in hydrogen producing non-axenic cultures of Rhodobacter sphaeroides RV. Int J Hydrogen Energy 27(11–12):1297–1302. doi:10.1016/S0360-3199(02)00119-2

    CAS  Google Scholar 

  • Koku H, Eroğlu I, Gündüz U, Yücel M, Türker L (2002) Aspects of the metabolism of hydrogen production by Rhodobacter sphaeroides. Int J Hydrogen Energy 27:1315–1329. doi:10.1016/S0360-3199(02)00127-1

    CAS  Google Scholar 

  • Kondo T, Arakawa M, Wakayama T, Miyake J (2002) Hydrogen production by combining two types of photosynthetic bacteria with different characteristics. Int J Hydrogen Energy 27(11–12):1303–1308. doi:10.1016/S0360-3199(02)00122-2

    CAS  Google Scholar 

  • Kondo T, Wakayama T, Miyake J (2006) Efficient hydrogen production using a multi-layered photobioreactor and a photosynthetic bacterium mutant with reduced pigment. Int J Hydrogen Energy 31(11):1522–1526. doi:10.1016/j.ijhydene.2006.06.019

    CAS  Google Scholar 

  • Kraemer JT, Bagley DM (2007) Improving the yield from fermentative hydrogen production. Biotechnol Lett 29:685–695. doi:10.1007/s10529-006-9299-9

    CAS  Google Scholar 

  • Kurokawa T, Shigeharu T (2005) Effects of formate on fermentative hydrogen production by Enterobacter aerogenes. Mar Biotechnol 7:112–118. doi:10.1007/s10126-004-3088-z

    CAS  Google Scholar 

  • Kvaalen E, Wankat PC, McKenzie BA (2006) Alcohol distillation: basic principles, equipment, performance relationships, and safety. www.ces.purdue.edu/extmedia/AE/AE-117.html, Accessed May 2008

  • Kyazze G, Dinsdale R, Guwy AJ, Hawkes FR, Premier GC, Hawkes DL (2007) Performance characteristics of a two-stage dark fermentative system producing hydrogen and methane continuously. Biotechnol Bioeng 97(4):759–770. doi:10.1002/bit.21297

    CAS  Google Scholar 

  • Larminie J, Dicks A (2003) Fuel cell systems explained, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Laurinavichene TV, Fedorov AS, Ghirardi ML, Siebert M, Tsygankov AA (2006) Demonstration of sustained hydrogen production by immobilised, sulfur-deprived Chlamydomonas reinhardtii cells. Int J Hydrogen Energy 31:659–667. doi:10.1016/j.ijhydene.2005.05.002

    CAS  Google Scholar 

  • Lee CM, Chen PC, Wang CC, Tung YC (2002) Photohydrogen production using purple nonsulfur bacteria with hydrogen fermentation reactor effluent. Int J Hydrogen Energy 27(11–12):1309–1313. doi:10.1016/S0360-3199(02)00102-7

    CAS  Google Scholar 

  • Levin DB (2004) Re: biohydrogen production: prospects and limitations to practical application-erratum. Int J Hydrogen Energy 29:1425–1426. doi:10.1016/j.ijhydene.2004.05.004

    CAS  Google Scholar 

  • Levin DB, Pitt L, Love M (2004) Biohydrogen production: prospects and limitations to practical application. Int J Hydrogen Energy 29:173–185. doi:10.1016/S0360-3199(03)00094-6

    CAS  Google Scholar 

  • Levin DB, Islam R, Cicek N, Sparling R (2006) Hydrogen production by Clostridium thermocellum 27405 from cellulosic biomass substrates. Int J Hydrogen Energy 31(11):1496–1503. doi:10.1016/j.ijhydene.2006.06.015

    CAS  Google Scholar 

  • Levin DB, Zhu H, Beland M, Cicek N, Holbein BE (2007) Potential for hydrogen and methane production from biomass residues in Canada. Bioresour Technol 98:654–660. doi:10.1016/j.biortech.2006.02.027

    CAS  Google Scholar 

  • Li H, Mustacci R, Knowles CJ, Skibar W, Sunderland G, Dalrymple I, Jackman SA (2004) An electrokinetic bioreactor: using direct electric current for enhanced lactic acid fermentation and product recovery. Tetrahedron 60:655–661. doi:10.1016/j.tet.2003.10.110

    CAS  Google Scholar 

  • Liang TM, Cheng SS, Wu KL (2002) Behavioral study on hydrogen fermentation reactor installed with silicone rubber membrane. Int J Hydrogen Energy 27(11–12):1157–1165. doi:10.1016/S0360-3199(02)00099-X

    CAS  Google Scholar 

  • Liessens J, Verstraete W (1986) Selective inhibitors for continuous non-axenic hydrogen production by Rhodobacter capsulatus. J Appl Bacteriol 61(6):547–557

    CAS  Google Scholar 

  • Lin C-Y, Lay CH (2005) A nutrient formation for fermentative hydrogen production using anaerobic sewage sludge microflora. Int J Hydrogen Energy 30:285–292. doi:10.1016/j.ijhydene.2004.03.002

    CAS  Google Scholar 

  • Lin Y, Tanaka S (2006) Ethanol fermentation from biomass resources: current state and prospects. Appl Microbiol Biotechnol 69(6):627–642. doi:10.1007/s00253-005-0229-x

    CAS  Google Scholar 

  • Lindblad P, Christensson K, Lindberg P, Fedorov A, Pinto F, Tsygankov A (2002) Photoproduction of H2 by wildtype Anabaena PCC 7120 and a hydrogen uptake deficient mutant: from laboratory experiments to outdoor culture. Int J Hydrogen Energy 27(11–12):1271–1281. doi:10.1016/S0360-3199(02)00111-8

    CAS  Google Scholar 

  • Ma F, Hanna MH (1999) Biodiesel production: a review. Bioresour Technol 70:1–15. doi:10.1016/S0960-8524(99)00025-5

    CAS  Google Scholar 

  • Mabee WE, Fraser EDG, McFarlane PN, Saddler JN (2006) Canadian biomass reserves for biorefining. Appl Biochem Biotechnol 129–132:22–40. doi:10.1385/ABAB:129:1:22

    Google Scholar 

  • Macaskie LE (2004) Biological hydrogen production from crops & sugar wastes. Final report, EPSRC project GR/S62406/01

  • Macaskie LE, Baxter-Plant VS, Creamer NJ, Humphries AC, Mikheenko IP, Mikheenko PM, Penfold DW, Yong P (2005) Applications of bacterial hydrogenases in waste decontamination, manufacture of novel bionanocatalysts and in sustainable energy. Biochem Soc Trans 33(Pt 1):76–79. doi:10.1042/BST0330076

    CAS  Google Scholar 

  • Macedo IC, Leal MRLV, Silva JEAR (2004) Assessment of greenhouse gas emissions in the production and use of fuel ethanol in Brazil, available at www.unica.com.br/i_pages/files/gee3.pdf

  • Macler BA, Bassham JA (1988) Carbon allocation in wild-type and Glc+ Rhodobacter sphaeroides under photoheterotrophic conditions. Appl Environ Microbiol 54(11):2737–2741

    CAS  Google Scholar 

  • Macler BA, Pelroy RA, Bassham JA (1979) Hydrogen formation in nearly stoichiometric amounts from glucose by a Rhodopseudomonas mutant. J Bacteriol 138(2):446–452

    CAS  Google Scholar 

  • Madamwar D, Garg N, Shah V (2000) Cyanobacterial hydrogen production. World J Microbiol Biotechnol 16:757–767. doi:10.1023/A:1008919200103

    CAS  Google Scholar 

  • Mandal B, Nath K, Das D (2006) Improvement of biohydrogen production under decreased partial pressure of H2 by Enterobacter cloacae. Biotechnol Lett 28:831–835. doi:10.1007/s10529-006-9008-8

    CAS  Google Scholar 

  • Martínez-Herrera J, Siddhuraju P, Francis G, Dávila-Ortíz G, Becker K (2006) Chemical composition, toxic/antimetabolic constituents, and effects of different treatments on their levels, in four provenances of Jatropha curcas L. from Mexico. Food Chem 96:80–89. doi:10.1016/j.foodchem.2005.01.059

    Google Scholar 

  • Masukawa H, Mochimaru M, Sakurai H (2002) Disruption of the uptake hydrogenase gene, but not of the bidirectional hydrogenase gene, leads to enhanced photobiological hydrogen production by the nitrogen-fixing cyanobacterium Anabaena sp. PCC 7120. Appl Microbiol Biotechnol 58(5):618–624

    CAS  Google Scholar 

  • McCormick DB (1998) Oxidation–reduction reactions. Encyclopedia of life sciences. Wiley, Chichester

    Google Scholar 

  • Melis A, Happe T (2004) Trails of green alga hydrogen research—from Hans Gaffron to new frontiers. Photosynth Res 80(1–3):401–409. doi:10.1023/B:PRES.0000030421.31730.cb

    CAS  Google Scholar 

  • Melis A, Melnicki MR (2006) Integrated biological hydrogen production. Int J Hydrogen Energy 31(11):1563–1573. doi:10.1016/j.ijhydene.2006.06.038

    CAS  Google Scholar 

  • Miura Y, Ohta S, Mano M, Miyamoto K (1986) Isolation and characterisation of a unicellular green alga exhibiting high activity in dark hydrogen production. Agric Biol Chem 50(11):2837–2844

    CAS  Google Scholar 

  • Miura Y, Saitoh C, Matsuoka S, Miyamoto K (1992) Stably sustained hydrogen production with high molar yield through a combination of a marine green alga and a photosynthetic bacterium. Biosci Biotechnol Biochem 56(5):751–754

    Article  CAS  Google Scholar 

  • Miyake J, Mao X-Y, Kawamura S (1984) Photoproduction of hydrogen from glucose by a co-culture of a photosynthetic bacterium and Clostridium butyricum. J Ferment Technol 62(6):531–535

    CAS  Google Scholar 

  • Miyake J, Miyake M, Asada Y (1999) Biotechnological hydrogen production: research for efficient light conversion. J Biotechnol 70:89–101. doi:10.1016/S0168-1656(99)00063-2

    CAS  Google Scholar 

  • Miyamoto K, Ohta S, Nawa Y, Mori Y, Miura Y (1987) Hydrogen production by a mixed culture of a green alga Chlamydomonas reinhardtii and a photosynthetic bacterium Rhodospirillum rubrum. Agric Biol Chem 51(5):1319–1324

    CAS  Google Scholar 

  • Mizuno O, Dinsdale R, Hawkes FR, Hawkes DL, Noike T (2000) Enhancement of hydrogen production from glucose by nitrogen gas sparging. Bioresour Technol 73:59–65. doi:10.1016/S0960-8524(99)00130-3

    CAS  Google Scholar 

  • Nakada E, Asada Y, Arai T, Miyake J (1995) Light penetration into cell suspensions of photosynthetic bacteria and relation to hydrogen production. J Ferment Bioeng 80(1):53–57. doi:10.1016/0922-338X(95)98176-L

    CAS  Google Scholar 

  • Nandi R, Sengupta S (1998) Microbial production of hydrogen: an overview. Crit Rev Microbiol 24(1):61–84. doi:10.1080/10408419891294181

    CAS  Google Scholar 

  • Nastari PM, Macedo IC, Szwarc A (2005) Observations on the draft document entitled “Potential for Biofuels for transport in developing countries”. The World Bank, Air Quality Thematic Group, p 8. http://www.unica.com.br/i_pages/files/ibm.pdf

  • Nath K, Das D (2003) Hydrogen from biomass. Curr Sci 85(3):265–271

    CAS  Google Scholar 

  • Nath K, Das D (2004a) Biohydrogen production as a potential energy source—present state-of-art. J Sci Ind Res (India) 63(9):729–738

    CAS  Google Scholar 

  • Nath K, Das D (2004b) Improvement of fermentative hydrogen production: various approaches. Appl Microbiol Biotechnol 65(5):520–529. doi:10.1007/s00253-004-1644-0

    CAS  Google Scholar 

  • Nath K, Kumar A, Das D (2005) Hydrogen production by Rhodobacter sphaeroides strain O.U.001 using spent media of Enterobacter cloacae strain DM11. Appl Microbiol Biotechnol 68:533–541. doi:10.1007/s00253-005-1887-4

    CAS  Google Scholar 

  • Nath K, Muthukumar M, Kumar A, Das D (2008) Kinetics of two-stage fermentation process for the production of hydrogen. Int J Hydrogen Energy 33(4):1195–1203. doi:10.1016/j.ijhydene.2007.12.011

    CAS  Google Scholar 

  • Nielsen AM, Amandusson H, Bjorklund R, Dannetun H, Ejlertsson J, Ekedahl L-G, Lundstrom I, Svensson BH (2001) Hydrogen production from organic waste. Int J Hydrogen Energy 26:547–550. doi:10.1016/S0360-3199(00)00125-7

    CAS  Google Scholar 

  • Nowak M (2004) Urban agriculture on the rooftop, Cornell University, available at www3.telus.net/public/a6a47567/roofgarden_thesis.pdf

  • Odom JM, Wall JD (1983) Photoproduction of H2 from cellulose by an anerobic bacterial culture. Appl Environ Microbiol 45(4):1300–1305

    CAS  Google Scholar 

  • Oh SE, Logan BE (2005) Hydrogen and electricity production from a food processing wastewater using fermentation and microbial fuel cell technologies. Water Res 39(19):4673–4682. doi:10.1016/j.watres.2005.09.019

    CAS  Google Scholar 

  • Oh Y-K, Seol E-H, Kim M-S, Park S (2004) Photoproduction of hydrogen from acetate by a chemoheterotrophic bacterium Rhodopseudomonas palustris P4. Int J Hydrogen Energy 29:1115–1121

    CAS  Google Scholar 

  • Ordal EJ, Halvorson HO (1939) A comparison of hydrogen production from sugars and formic acid by normal and variant strains of Escherichia coli. J Bacteriol 38:199–220

    CAS  Google Scholar 

  • Öztürk Y, Yücel M, Daldal F, Mandaci S, Gündüz U, Türker L, Eroğlu I (2006) Hydrogen production by using Rhodobacter capsulatus mutants with genetically modified electron transfer chains. Int J Hydrogen Energy 31(11):1545–1552. doi:10.1016/j.ijhydene.2006.06.042

    Google Scholar 

  • Park W, Hyun SH, Oh SE, Logan BE, Kim IS (2005) Removal of headspace CO2 increases biological hydrogen production. Environ Sci Technol 39(12):4416–4420. doi:10.1021/es048569d

    CAS  Google Scholar 

  • Penfold DW, Forster CF, Macaskie LE (2003) Increased hydrogen production by Escherichia coli strain HD701 in comparison with the wild-type parent strain MC4100. Enzyme Microb Technol 33(2–3):185–189. doi:10.1016/S0141-0229(03)00115-7

    CAS  Google Scholar 

  • Pimentel D (2001) The limitations of biomass energy. In: Meyers R (ed) Encyclopedia of physical science, technology, 3rd edn. Academic Press, San Diego, pp 159–171

    Google Scholar 

  • Polle JEW, Kanakagiri S, Jin E, Masuda T, Melis A (2002) Truncated chlorophyll antenna size of the photosystems—a practical method to improve microalgal productivity and hydrogen production in mass culture. Int J Hydrogen Energy 27(11–12):1257–1264. doi:10.1016/S0360-3199(02)00116-7

    CAS  Google Scholar 

  • Redwood MD, Macaskie LE (2006) A two-stage, two-organism process for biohydrogen from glucose. Int J Hydrogen Energy 31(11):1514–1521. doi:10.1016/j.ijhydene.2006.06.018

    CAS  Google Scholar 

  • Redwood MD, Macaskie LE (2007a) Method and apparatus for biohydrogen production. British patent application no. 0705583.3, UK

  • Redwood MD, Macaskie LE (2007b) Efficient bio-H2 and PEM-FC catalyst. In: Proceedings of the 7th hydrogen-power and theoretical engineering solutions international symposium (HyPoThESIS VII), Merida. CICY ISBN:968-6114-21-1

  • Redwood MD, Mikheenko IP, Sargent F, Macaskie LE (2007) Dissecting the roles of E. coli hydrogenases in biohydrogen production. FEMS Microbiol Lett 278:48–55. doi:10.1111/j.1574-6968.2007.00966.x

    Google Scholar 

  • Ren N, Li J, Wang Y, Liu S (2006) Biohydrogen production from molasses by anaerobic fermentation with a pilot-scale bioreactor system. Int J Hydrogen Energy 31:2147–2157. doi:10.1016/j.ijhydene.2006.02.011

    CAS  Google Scholar 

  • Rocha JS, Barbosa MJ, Wijffels RH (2001) Hydrogen production by photoheterotrophic bacteria: culture media, yields and efficiencies. In: Miyake J, Matsunaga T, San Pietro A (eds) Biohydrogen II: an approach to environmentally acceptable technology. Pergamon, Oxford, pp 3–32

    Google Scholar 

  • Roe AJ, McLaggan D, Davidson I, O’Byrne C, Booth IR (1998) Perturbation of anion balance during inhibition of growth of Echerichia coli by weak acids. J Bacteriol 180(4):767–772

    CAS  Google Scholar 

  • Rogers PL, Jeon YJ, Svenson CJ (2005) Application of biotechnology to industrial sustainability. Process Saf Environ Prot 83(B6):499–503

    CAS  Google Scholar 

  • Sakurai H, Masukawa H (2007) Promoting R & D in photobiological hydrogen production utilizing mariculture-raised cyanobacteria. Mar Biotechnol 9:128–145. doi:10.1007/s10126-006-6073-x

    CAS  Google Scholar 

  • Sasikala K, Ramana CV, Rao PR, Subrahmanyam M (1990) Effect of gas phase on the photoproduction of hydrogen and substrate conversion efficiency on the photosynthetic bacterium Rhodobacter sphaeroides O.U. 001. Int J Hydrogen Energy 15(11):795–797. doi:10.1016/0360-3199(90)90015-Q

    CAS  Google Scholar 

  • Sasikala K, Ramana CV, Subrahmanyam M (1991) Photoproduction of hydrogen from wastewater of a lactic acid fermentation plant by a purple non-sulfur photosynthetic bacterium Rhodobacter sphaeroides. Indian J Exp Biol 29:74–75

    CAS  Google Scholar 

  • Sasikala K, Ramana CV, Rao PR (1992) Photoproduction of hydrogen from the waste water of a distillery by Rhodobacter sphaeroides O.U. 001. Int J Hydrogen Energy 17(1):23–27. doi:10.1016/0360-3199(92)90217-K

    CAS  Google Scholar 

  • Sasikala C, Ramana CV, Prasad GS (1994a) H2 production by mixed cultures. World J Microbiol Biotechnol 10(2):221–223. doi:10.1007/BF00360892

    CAS  Google Scholar 

  • Sasikala C, Ramana CV, Rao PR (1994b) Nitrogen fixation by Rhodopseudomonas palustris OU 11 with aromatic compounds as carbon source/electron donors. FEMS Microbiol Lett 122:75–78. doi:10.1111/j.1574-6968.1994.tb07146.x

    CAS  Google Scholar 

  • Sasikala K, Ramana CV, Rao PR, Kovacs KL (1995) Anoxygenic phototrophic bacteria: physiology and advances in hydrogen production technology. Adv Appl Microbiol 38:211–295. doi:10.1016/S0065-2164(08)70217-X

    Google Scholar 

  • Sauter M, Bohm R, Bock A (1992) Mutational analysis of the operon (hyc) determining hydrogenase-3 formation in Escherichia coli. Mol Microbiol 6(11):1523–1532. doi:10.1111/j.1365-2958.1992.tb00873.x

    CAS  Google Scholar 

  • Schnoor JL (2006) Biofuels and the environment. Environ Sci Technol 40(13):4024

    Google Scholar 

  • Shi X-Y, Yu Q-H (2006) Continuous production of hydrogen from mixed volatile fatty acids with Rhodopseudomonas capsulata. Int J Hydrogen Energy 31:1641–1647. doi:10.1016/j.ijhydene.2005.12.008

    CAS  Google Scholar 

  • Sode K, Watanabe M, Makimoto H, Tomiyama M (1999) Construction and characterisation of fermentative lactate dehydrogenase E. coli mutant and its potential for bacterial hydrogen production. Appl Biochem Biotechnol 77–79:317–323. doi:10.1385/ABAB:77:1-3:317

    Google Scholar 

  • Sode K, Yamamoto S, Tomiyama M (2001) Metabolic engineering approaches for the improvement of bacterial hydrogen production based on Escherichia coli mixed acid fermentation. In: Miyake J, Matsunaga T, San Pietro A (eds) Biohydrogen II: an approach to environmentally acceptable technology. Pergamon, Oxford, pp 195–204

    Google Scholar 

  • Splendiani A, Nicolella C, Livingston AG (2003) A novel biphasic extractive membrane bioreactor for minimization of membrane-attached biofilms. Biotechnol Bioeng 83(1):8–19. doi:10.1002/bit.10643

    CAS  Google Scholar 

  • Srivastava A, Prasad R (2000) Triglycerides-based diesel fuels. Renew Sustain Energy Rev 4(2):111–133. doi:10.1016/S1364-0321(99)00013-1

    CAS  Google Scholar 

  • Staubmann R, Foidl G, Foidl N, Guebitz GM, Lafferty R, Valencia-Arbizu VM, Walter S (1997) Biogas production from Jatropha curcas press-cake. Appl Biochem Biotechnol 63–65:457–467. doi:10.1007/BF02920446

    Google Scholar 

  • Stephenson M, Stickland LH (1932) Hydrogenlyases: bacterial enzymes liberating molecular hydrogen. Biochem J 26:712–724

    CAS  Google Scholar 

  • Stern N (2006) Stern review executive summary. New Economics Foundation. Available at news.bbc.co.uk/1/shared/bsp/hi/pdfs/30_10_06_exec_sum.pdf

  • Tabita FR (1995) The biochemistry and metabolic regulation of carbon metabolism and CO2 fixation in purple bacteria. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 885–914

    Google Scholar 

  • Taillez P, Girard H, Longin R, Beguin P, Millet J (1983) Cellulose fermentation by an asporogenic mutant and an ethanol-tolerant mutant of Clostridium thermocellum. Appl Environ Microbiol 55(1):203–206

    Google Scholar 

  • Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wunschiers R, Lindblad P (2002) Hydrogenases and hydrogen metabolism in cyanobacteria. Microbiol Mol Biol Rev 66(1):1–20. doi:10.1128/MMBR.66.1.1-20.2002

    CAS  Google Scholar 

  • Tanisho S, Ishiwata Y (1995) Continuous hydrogen production from molasses by fermentation using urethane foam as a support of flocks. Int J Hydrogen Energy 20(7):541–545. doi:10.1016/0360-3199(94)00101-5

    CAS  Google Scholar 

  • Tanisho S, Kuromoto M, Kadokura N (1998) Effect of CO2 removal on hydrogen evolution by fermentation. Int J Hydrogen Energy 23(7):559–563. doi:10.1016/S0360-3199(97)00117-1

    CAS  Google Scholar 

  • Tao Y, Chen Y, Wu Y, He Y, Zhou Z (2007) High hydrogen yield from a two-step process of dark and photo-fermentation of sucrose. Int J Hydrogen Energy 32:200–206. doi:10.1016/j.ijhydene.2006.06.034

    CAS  Google Scholar 

  • Tao Y, He Y, Wu Y, Liu F, Li X, Zong W, Zhou Z (2008) Characteristics of a new photosynthetic bacterial strain for hydrogen production and its application in wastewater treatment. Int J Hydrogen Energy 33(3):963–973. doi:10.1016/j.ijhydene.2007.11.021

    CAS  Google Scholar 

  • Teplyakov VV, Gassanova LG, Sostina EG, Slepova EV, Modigell M, Netrusov AI (2002) Lab-scale bioreactor integrated with active membrane system for hydrogen production: experience and prospects. Int J Hydrogen Energy 27:1149–1155. doi:10.1016/S0360-3199(02)00093-9

    CAS  Google Scholar 

  • Thangaraj A, Kulandaivelu G (1994) Biological hydrogen photoproduction using dairy and sugarcane wastewaters. Bioresour Technol 48:9–12. doi:10.1016/0960-8524(94)90127-9

    CAS  Google Scholar 

  • Thauer R (1977) Limitation of microbial H2-formation via fermentation. In: Schlegel HG, Barnea J (eds) Microbial energy conversion. Pergamon, Oxford, pp 201–204

    Google Scholar 

  • Tiwari AK, Kumar A, Raheman H (2007) Biodiesel production from jatropha oil (Jatropha curcas) with high free fatty acids: an optimized process. Biomass Bioenergy 31:569–575. doi:10.1016/j.biombioe.2007.03.003

    Google Scholar 

  • Tosatto SCE, Toppo S, Donatella C, Giacometti GM, Costantini P (2008) Comparative analysis of [FeFe] hydrogenase from Thermotogales indicates the molecular basis of resistance to oxygen inactivation. Int J Hydrogen Energy 33(2):570–578. doi:10.1016/j.ijhydene.2007.10.010

    CAS  Google Scholar 

  • Troshina O, Serebryakova L, Sheremetieva M, Lindblad P (2002) Production of H2 by the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermentation. Int J Hydrogen Energy 27(11–12):1283–1289. doi:10.1016/S0360-3199(02)00103-9

    CAS  Google Scholar 

  • Tsygankov AA (2001) Laboratory scale photobioreactors. Appl Biochem Microbiol 37(4):333–341. doi:10.1023/A:1010266116747

    CAS  Google Scholar 

  • Tsygankov A (2007a) Nitrogen-fixing cyanobacteria: a review. Appl Biochem Microbiol 43(3):250. doi:10.1134/S0003683807030040

    CAS  Google Scholar 

  • Tsygankov AA (2007b) Biological generation of hydrogen. Russ J Gen Chem 77(4):685–693. doi:10.1134/S1070363207040317

    CAS  Google Scholar 

  • Tsygankov AA, Fedorov AS, Laurinavichene TV, Gogotov IN, Rao KK, Hall DO (1998) Actual and potential rates of hydrogen photoproduction by continuous culture of the purple non-sulphur bacterium Rhodobacter capsulatus. Appl Microbiol Biotechnol 49(1):102–107. doi:10.1007/s002530051144

    CAS  Google Scholar 

  • Tsygankov AA, Fedorov AS, Kosourov SN, Rao KK (2002) Hydrogen production by cyanobacteria in an automated outdoor photobioreactor under aerobic conditions. Biotechnol Bioeng 80(7):777–783. doi:10.1002/bit.10431

    CAS  Google Scholar 

  • Turkarslan S, Yiğit OD, Aslan K, Eroğlu I, Gündüz U (1997) Photobiological hydrogen production by R. sphaeroides O.U 001 by utilisation of waste water from milk industry. International conference on biological hydrogen production, Plenum, New York

  • Ueno Y, Kawai T, Sato S, Otsuka S, Morimoto S (1995) Biological production of hydrogen from cellulose by natural anaerobic microflora. J Ferment Bioeng 97(4):395–397. doi:10.1016/0922-338X(95)94005-C

    Google Scholar 

  • Valdez-Vazquez I, Sparling R, Risbey D, Rinderknecht-Seijas N, Poggi-Varraldo HM (2005) Hydrogen generation via anaerobic fermentations of paper mill wastes. Bioresour Technol 96:1907–1913. doi:10.1016/j.biortech.2005.01.036

    CAS  Google Scholar 

  • Valdez-Vazquez I, Rios-Leal E, Carmona-Martinez A, Munoz-Paez KM, Poggi-Varaldo HM (2006) Improvement of biohydrogen production from solid wastes by intermittent venting and gas flushing of batch reactors headspace. Environ Sci Technol 40:3409–3415. doi:10.1021/es052119j

    CAS  Google Scholar 

  • Van Ginkel S, Logan BE (2005) Inhibition of biohydrogen production by undissociated acetic and butyric acids. Environ Sci Technol 39:9350–9356. doi:10.1021/es0510515

    Google Scholar 

  • Van Groenestijn JW, Hazewinkel JHO, Nienoord M, Bussmann PJT (2002) Energy aspects of biological hydrogen production in high rate bioreactors operated in the thermophilic temperature range. Int J Hydrogen Energy 27(11–12):1141–1147. doi:10.1016/S0360-3199(02)00096-4

    Google Scholar 

  • Van Haaster DJ, Hagedoorn PL, Jongejan JA, Hagen WR (2005) On the relationship between affinity for molecular hydrogen and the physiological directionality of hydrogenases. Biochem Soc Trans 33(1):12–14. doi:10.1042/BST0330012

    Google Scholar 

  • Van Niel EWJ, Budde MAW, de Haas GG, van der Wal FJ, Claassen PAM, Stams AJM (2002) Distinctive properties of high hydrogen producing extreme thermophiles, Caldicellulosiruptor saccharolyticus and Thermotoga elfii. Int J Hydrogen Energy 27(11–12):1390–1398

    Google Scholar 

  • Van Niel EWJ, Claassen PAM, Stams AJM (2003) Substrate and product inhibition of hydrogen production by the extreme thermophile, Caldicellulosiruptor saccharolyticus. Biotechnol Bioeng 81(3):255–262. doi:10.1002/bit.10463

    Google Scholar 

  • Van Ooteghem SA, Jones A, van der Lelie D, Dong B, Mahajan D (2004) H2 production and carbon utilization by Thermotoga neapolitana under anaerobic and microaerobic growth conditions. Biotechnol Lett 26(15):1223–1232. doi:10.1023/B:BILE.0000036602.75427.88

    Google Scholar 

  • Vardar-Schara G, Maeda T, Wood TK (2008) Metabolically engineered bacteria for producing hydrogen via fermentation. Microb Biotechnol 1(2):107–125

    CAS  Google Scholar 

  • Vasilyeva L, Miyake M, Khatipov E, Wakayama T, Sekine M, Hara M, Nakada E, Asada Y, Miyake J (1999) Enhanced hydrogen production by a mutant of R. sphaeroides having an altered light-harvesting system. J Biosci Bioeng 87(5):619–624. doi:10.1016/S1389-1723(99)80124-8

    CAS  Google Scholar 

  • Vignais PM, Colbeau M, Willison JC, Jouanneau Y (1985) Hydrogenase, nitrogenase, and hydrogen metabolism in the photosynthetic bacteria. Adv Microb Physiol 26:155–234. doi:10.1016/S0065-2911(08)60397-5

    CAS  Google Scholar 

  • Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25(4):455–501

    CAS  Google Scholar 

  • Vincenzini M, Marchini A, Ena A, De Philippis R (1997) H2 and poly-β-hydroxybutyrate, two alternative chemicals from purple non sulfur bacteria. Biotechnol Lett 19(8):759–762. doi:10.1023/A:1018336209252

    CAS  Google Scholar 

  • Wakayama T, Miyake J (2001) Hydrogen from biomass. In: Miyake J, Matsunaga T, San Pietro A (eds) Biohydrogen II: an approach to environmentally acceptable technology. Pergamon, Oxford, pp 3–32

    Google Scholar 

  • Wakayama T, Miyake J (2002) Light shade bands for the improvement of solar hydrogen production efficiency by Rhodobacter sphaeroides RV. Int J Hydrogen Energy 27:1495–1500. doi:10.1016/S0360-3199(02)00088-5

    CAS  Google Scholar 

  • Wakayama T, Nakada E, Asada Y, Miyake J (2000) Effect of light/dark cycle on bacterial hydrogen production by Rhodobacter sphaeroides RV—from hour to second range. Appl Biochem Biotechnol 84–86:431–440. doi:10.1385/ABAB:84-86:1-9:431

    Google Scholar 

  • Wall JD, Gest H (1979) Derepression of nitrogenase activity in glutamine auxotrophs of Rhodopseudomonas capsulata. J Bacteriol 137(3):1459–1463

    CAS  Google Scholar 

  • Weetall HH, Sharma BP, Detar CC (1989) Photometabolic production of hydrogen from organic substrates by free and immobilised mixed cultures of Rhodospirillum rubrum and Klebsiella pneumoniae. Biotechnol Bioeng 23:605–614. doi:10.1002/bit.260230310

    Google Scholar 

  • Willison JC, Madern D, Vignais PM (1984) Increased photoproduction of hydrogen by non-autotrophic mutants of Rhodopseudomonas capsulata. Biochem J 219(2):593–600

    CAS  Google Scholar 

  • Worin NA, Lissolo T, Colbeau A, Vignais PM (1996) Increased H2 photoproduction by Rhodobacter capsulatus strains deficient in uptake hydrogenase. J Mar Biotechnol 4:28–33

    Google Scholar 

  • Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron-transport. Plant Physiol 117:129–139. doi:10.1104/pp.117.1.129

    CAS  Google Scholar 

  • Yagi K, Maeda I, Idehara K, Miura Y, Akano T, Fukatu K, Ikuta Y, Nakamura HK (1994) Removal of inhibition by ammonium ion in nitrogenase-dependent hydrogen evolution of a marine photosynthetic bacterium, Rhodopseudomonas sp strain W-1s. Appl Biochem Biotechnol 45–46:429–436. doi:10.1007/BF02941817

    Google Scholar 

  • Yetis M, Gündüz U, Eroğlu I, Yücel M, Türker L (2000) Photoproduction of hydrogen from sugar refinery wastewater by Rhodobacter sphaeroides O.U. 001. Int J Hydrogen Energy 25:1035–1041. doi:10.1016/S0360-3199(00)00027-6

    CAS  Google Scholar 

  • Yiğit OD, Gündüz U, Türker L, Yücel M, Eroğlu I (1999) Identification of by-products in hydrogen producing bacteria; Rhodobacter sphaeroides O.U. 001 grown in the waste water of a sugar refinery. J Biotechnol 70:125–131. doi:10.1016/S0168-1656(99)00066-8

    Google Scholar 

  • Ying Li R, Zhang T, Fang HHP (2008) Characteristics of a phototrophic sludge producing hydrogen from acetate and butyrate. Int J Hydrogen Energy 33(9):2147–2155. doi:10.1016/j.ijhydene.2008.02.055

    Google Scholar 

  • Yokoi H, Mori S, Hirose J, Hayashi S, Takasaki Y (1998) H2 production from starch by a mixed culture of Clostridium butyricum and Rhodobacter sp. M-19. Biotechnol Lett 20(9):895–899. doi:10.1023/A:1005327912678

    CAS  Google Scholar 

  • 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):58–63. doi:10.1263/jbb.91.58

    CAS  Google Scholar 

  • Yokoi H, Maki R, Hirose J, Hayashi S (2002) Microbial production of hydrogen from starch-manufacturing wastes. Biomass Bioenergy 22:389–395. doi:10.1016/S0961-9534(02)00014-4

    CAS  Google Scholar 

  • Yoon JH, Shin JH, Kim M-S, Sim SJ, Park TH (2006) Evaluation of conversion efficiency of light to hydrogen energy by Anabaena variabilis. Int J Hydrogen Energy 31:721–727. doi:10.1016/j.ijhydene.2005.06.023

    CAS  Google Scholar 

  • Yoshida A, Nishimura T, Kawaguchi H, Inui M, Yukuwa H (2005) Enhanced hydrogen production from formic acid by formate hydrogen lyase-overexpressing Escherichia coli strains. Appl Environ Microbiol 71(11):6762–6768. doi:10.1128/AEM.71.11.6762-6768.2005

    CAS  Google Scholar 

  • Yoshino F, Ikeda H, Masukawa H, Sakurai H (2007) High photobiological hydrogen production activity of a Nostoc sp. PCC 7422 uptake hydrogenase-deficient mutant with high nitrogenase activity. Mar Biotechnol NY 9(1):101–112. doi:10.1007/s10126-006-6035-3

    CAS  Google Scholar 

  • Yun S-I, Ohta Y (2005) Removal of volatile fatty acids with immobilised Rhodococcus sp. B261. Bioresour Technol 96:41–46. doi:10.1016/j.biortech.2004.03.006

    CAS  Google Scholar 

  • Zacchi G, Axelsson A (1989) Economic evaluation of preconcentration in product and of ethanol from dilute sugar solutions. Biotechnol Bioeng 34:223–233. doi:10.1002/bit.260340211

    CAS  Google Scholar 

  • Zhu H, Miyake J, Tsygankov AA, Asada Y (1995) Hydrogen production from highly concentrated organic wastewater by photosynthetic bacteria & anaerobic bacteria. Water Treat 10:61–68

    Google Scholar 

  • Zhu H, Suzuki T, Tsygankov AA, Asada Y, Miyake J (1999a) Hydrogen production from tofu waste water by Rhodobacter sphaeroides immobilised in agar gels. Int J Hydrogen Energy 24:305–310. doi:10.1016/S0360-3199(98)00081-0

    CAS  Google Scholar 

  • Zhu H, Wakayama T, Suzuki T, Asada Y, Miyake J (1999b) Entrapment of Rhodobacter sphaeroides in cationic polymer/agar gels for hydrogen production in the presence of NH4 +. J Biosci Bioeng 88(5):507–512. doi:10.1016/S1389-1723(00)87667-7

    CAS  Google Scholar 

  • Zhu H, Wakayama T, Asada Y, Miyake J (2001) Hydrogen production by four cultures with participation by anoxygenic photosynthetic bacterium and anaerobic bacterium in the presence of NH4 +. Int J Hydrogen Energy 26(11):1149–1154. doi:10.1016/S0360-3199(01)00038-6

    CAS  Google Scholar 

  • Zhu HG, Ueda S, Asada Y, Miyake J (2002) Hydrogen production as a novel process of wastewater treatment—studies on tofu wastewater with entrapped R. sphaeroides and mutagenesis. Int J Hydrogen Energy 27(11-12):1349–1357. doi:10.1016/S0360-3199(02)00118-0

    CAS  Google Scholar 

  • Zinchenko VV, Kopteva AV, Belavina NV, Mitronova TN, Frolova VD, Shestakov SV (1991) The study of Rhodobacter sphaeroides mutants of different type with derepressed nitrogenase. Genetika 27(6):991–999

    CAS  Google Scholar 

  • Zinchenko VV, Babykin M, Glaser V, Mekhedov S, Shestakov SV (1997) Mutation in ntrC gene leading to the derepression of nitrogenase synthesis in Rhodobacter sphaeroides. FEMS Microbiol Lett 147:57–61. doi:10.1111/j.1574-6968.1997.tb10220.x

    CAS  Google Scholar 

  • Zurrer H, Bachofen R (1979) Hydrogen production by the photosynthetic bacterium Rhodospirillum rubrum. Appl Environ Microbiol 37(5):789–793

    CAS  Google Scholar 

  • Züttel A (2004) Hydrogen storage methods. Naturwissenschaften 91(4):157–172. doi:10.1007/s00114-004-0516-x

    Google Scholar 

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Acknowledgments

We acknowledge the financial support of the Biotechnology and Biological Sciences Research Council (Grant no. BB/C516128/1 and studentship no. 10703 to MDR), Engineering and Physical Sciences Research Council (Grant no. EP/E03488/1) and Department of Environment, Food and Rural Affairs (Contract no. NTFUN2). LEM was supported by a BBSRC/Royal Society Industrial Fellowship in partnership with C-Tech Innovation Ltd.

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  1. School of Biosciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK

    Mark D. Redwood, Marion Paterson-Beedle & Lynne E. Macaskie

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  1. Mark D. Redwood
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Correspondence to Mark D. Redwood.

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Redwood, M.D., Paterson-Beedle, M. & Macaskie, L.E. Integrating dark and light bio-hydrogen production strategies: towards the hydrogen economy. Rev Environ Sci Biotechnol 8, 149–185 (2009). https://doi.org/10.1007/s11157-008-9144-9

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