Recent trends on the development of photobiological processes and photobioreactors for the improvement of hydrogen production

Hydrogen production through biological routes is promising because they are environmentally friendly. Hydrogen production through biophotolysis or photofermentation is usually a two stage process. In the first stage CO2 is utilized for biomass production which is followed by hydrogen production in the second stage in anaerobic/sulfur-deprived conditions. In addition, one-stage photobiological hydrogen production process can be achieved using selected cyanobacterial strains. The major challenges confronting the large scale production of biomass/hydrogen are limited not only on the performance of the photobioreactors in which light penetration in dense cultures is a major bottleneck but also on the characteristics of the organisms. Other dependable factors include area/ volume (A/V) ratio, mode of agitation, temperature and gas exchange. Photobioreactors of different geometries are reported for biohydrogen production: Tubular, Flat plate, Fermentor type etc. Every reactor has its own advantages and disadvantages. Airlift, helical tubular and flat plate reactors are found most suitable with respect to biomass production. These bioreactors may be employed for hydrogen production with necessary modifications to overcome the existing bottlenecks like gas hold up, oxygen toxicity and poor agitation. This review article attempts to focus on existing photobioreactors with respect to biomass generation and hydrogen production and the steps taken to improve its performance through engineering innovation that definitely help in the future design and construction of photobioreactors.

[1]  Halil Berberoglu,et al.  Effect of nutrient media on photobiological hydrogen production by Anabaena variabilis ATCC 29413 , 2008 .

[2]  R. Bachofen,et al.  Aspects of growth and hydrogen production of the photosynthetic bacterium Rhodospirillum rubrum in continuous culture , 1982 .

[3]  W. E. Krumbein,et al.  Temporal separation of nitrogen fixation and photosynthesis in the filamentous, non-heterocystous cyanobacterium Oscillatoria sp. , 1987, Archives of Microbiology.

[4]  K. Sasikala,et al.  Anoxygenic Phototrophic Bacteria: Physiology and Advances in Hydrogen Production Technology , 1993 .

[5]  J. Ogbonna,et al.  Development of Efficient Large-Scale Photobioreactors , 1998 .

[6]  Mario R. Tredici,et al.  Novel photobioreactors for the mass cultivation of Spirulina spp. , 1993 .

[7]  R. Smith,et al.  Effect of inorganic carbon on photoautotrophic growth of microalga Chlorococcum littorale , 2009, Biotechnology progress.

[8]  P. Lindblad,et al.  Evidence for transcription of three genes with characteristics of hydrogenases in the green alga Chlamydomonas noctigama , 2010 .

[9]  H. Saiki,et al.  Investigation of photobioreactor design for enhancing the photosynthetic productivity of microalgae. , 2000, Biotechnology and bioengineering.

[10]  E. Greenbaum,et al.  A new oxygen sensitivity and its potential application in photosynthetic H2 production , 2003 .

[11]  Contreras,et al.  Interaction between CO2-mass transfer, light availability, and hydrodynamic stress in the growth of phaeodactylum tricornutum in a concentric tube airlift photobioreactor , 1998, Biotechnology and bioengineering.

[12]  L. Stal,et al.  Oxygen protection of nitrogenase in the aerobically nitrogen fixing, non-heterocystous cyanobacterium Oscillatoria sp. , 1985, Archives of Microbiology.

[13]  Cecilia Faraloni,et al.  Increased hydrogen photoproduction by means of a sulfur-deprived Chlamydomonas reinhardtii D1 protein mutant , 2009 .

[14]  Anja Doebbe,et al.  Functional integration of the HUP1 hexose symporter gene into the genome of C. reinhardtii: Impacts on biological H(2) production. , 2007, Journal of biotechnology.

[15]  G. C. Zittelli,et al.  A Tubular Integral Gas Exchange Photobioreactor for Biological Hydrogen Production , 1998 .

[16]  Shozo Kawasaki,et al.  Biological H 2 production using a novel light-induced and diffused photoreactor , 1997 .

[17]  Michael C. Flickinger,et al.  Encyclopedia of bioprocess technology : fermentation, biocatalysis, and bioseparation , 1999 .

[18]  G. Bernát,et al.  Towards efficient hydrogen production: the impact of antenna size and external factors on electron transport dynamics in Synechocystis PCC 6803 , 2009, Photosynthesis Research.

[19]  Toshiro Hirai,et al.  Enhancement of hydrogen production by a photosynthetic bacterium mutant with reduced pigment. , 2002, Journal of bioscience and bioengineering.

[20]  Kai Zhang,et al.  Optimized aeration by carbon dioxide gas for microalgal production and mass transfer characterization in a vertical flat-plate photobioreactor , 2002, Bioprocess and biosystems engineering.

[21]  K. Sasaki Hydrogen and 5-Aminolevulinic Acid Production by Photosynthetic Bacteria , 1998 .

[22]  S. Miyachi,et al.  Evaluation of a vertical flat-plate photobioreactor for outdoor biomass production and carbon dioxide bio-fixation: effects of reactor dimensions, irradiation and cell concentration on the biomass productivity and irradiation utilization efficiency , 2001, Applied Microbiology and Biotechnology.

[23]  Jeffrey J. Chalmers,et al.  Cells and bubbles in sparged bioreactors , 2004, Cytotechnology.

[24]  Kisay Lee,et al.  Influence of Nitrate Feeding on Carbon Dioxide Fixation by Microalgae , 2006, Journal of environmental science and health. Part A, Toxic/hazardous substances & environmental engineering.

[25]  E. Becker Microalgae: Biotechnology and Microbiology , 1994 .

[26]  N. Bishop,et al.  Interrelation of the mechanisms for oxygen and hydrogen evolution in adapted algae , 1963 .

[27]  H Guterman,et al.  A flat inclined modular photobioreactor for outdoor mass cultivation of photoautotrophs , 2000, Biotechnology and bioengineering.

[28]  Jack Rubin,et al.  FERMENTATIVE AND PHOTOCHEMICAL PRODUCTION OF HYDROGEN IN ALGAE , 1942, The Journal of general physiology.

[29]  G. C. Zittelli,et al.  Efficiency of sunlight utilization: tubular versus flat photobioreactors , 1998, Biotechnology and bioengineering.

[30]  P. Lindblad,et al.  H2 production from marine and freshwater species of green algae during sulfur deprivation and considerations for bioreactor design , 2008 .

[31]  I. Eroglu,et al.  Aspects of the metabolism of hydrogen production by Rhodobacter sphaeroides , 2002 .

[32]  J. Magnin,et al.  Increasing biohydrogen production by metabolic engineering , 2006 .

[33]  R. Moezelaar,et al.  Fermentation and Sulfur Reduction in the Mat-Building Cyanobacterium Microcoleus chthonoplastes , 1996, Applied and environmental microbiology.

[34]  Y. Asada,et al.  Heterologous expression of clostridial hydrogenase in the Cyanobacterium synechococcus PCC7942. , 2000, Biochimica et biophysica acta.

[35]  I. N. Gogotov,et al.  Hydrogen production by model systems including hydrogenases from phototrophic bacteria , 1991 .

[36]  Paula Tamagnini,et al.  Hydrogenases and Hydrogen Metabolism of Cyanobacteria , 2002, Microbiology and Molecular Biology Reviews.

[37]  Z. Su,et al.  An Effective Device for Gas–Liquid Oxygen Removal in Enclosed Microalgae Culture , 2010, Applied biochemistry and biotechnology.

[38]  Ufuk Gündüz,et al.  Improved hydrogen production by uptake hydrogenase deficient mutant strain of Rhodobacter sphaeroides O.U.001 , 2008 .

[39]  M. Mandrand,et al.  Microbial hydrogenases: primary structure, classification, signatures and phylogeny. , 1993, FEMS microbiology reviews.

[40]  M. Modigell,et al.  DEVELOPMENT OF PHOTOBIOREACTORS FOR ANOXYGENIC PRODUCTION OF HYDROGEN BY PURPLE BACTERIA , 2009 .

[41]  Kadir Aslan,et al.  Substrate consumption rates for hydrogen production by Rhodobacter sphaeroides in a column photobioreactor , 1999 .

[42]  J. Benemann,et al.  Vertical tubular reactor for microalgae cultivation , 1988, Biotechnology Letters.

[43]  C. Dussap,et al.  A fully predictive model for one-dimensional light attenuation by Chlamydomonas reinhardtii in a torus photobioreactor. , 2005, Biotechnology and bioengineering.

[44]  Hadiyanto,et al.  Overcoming shear stress of microalgae cultures in sparged photobioreactors , 2004, Biotechnology and bioengineering.

[45]  Yusuf Chisti,et al.  Bubble‐column and airlift photobioreactors for algal culture , 2000 .

[46]  Y. Asada,et al.  Fermentative Metabolism to Produce Hydrogen Gas and Organic Compounds in a Cyanobacterium, Spirulina platensis , 1997 .

[47]  R. El-Shishtawy,et al.  Study on the Behavior of Production and Uptake of Photobiohydrogen by Photosynthetic Bacterium Rhodobacter sphaeroides RV , 1998 .

[48]  B. Palsson,et al.  High‐density photoautotrophic algal cultures: Design, construction, and operation of a novel photobioreactor system , 1991, Biotechnology and bioengineering.

[49]  Debabrata Das,et al.  Hydrogen production by biological processes: a survey of literature , 2001 .

[50]  A. McDowall,et al.  Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. , 2007, Plant biotechnology journal.

[51]  I. Eroglu,et al.  Continuous Hydrogen Production by Rhodobacter sphaeroides O.U.001 , 1998 .

[52]  René H. Wijffels,et al.  Photobiological hydrogen production: photochemical efficiency and bioreactor design , 2002 .

[53]  A. Kiperstok,et al.  Comparative energy life-cycle analyses of microalgal biomass production in open ponds and photobioreactors. , 2010, Bioresource technology.

[54]  A Borowitzka Michael Closed algal photobioreactors : Design considerations for large-scale systems , 1996 .

[55]  A. Hemschemeier,et al.  The exceptional photofermentative hydrogen metabolism of the green alga Chlamydomonas reinhardtii. , 2005, Biochemical Society transactions.

[56]  J. Naber,et al.  Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. , 1993, European journal of biochemistry.

[57]  Anish Kumar,et al.  Hydrogen production by Rhodobacter sphaeroides strain O.U.001 using spent media of Enterobacter cloacae strain DM11 , 2005, Applied Microbiology and Biotechnology.

[58]  Olaf Kruse,et al.  Improved Photobiological H2 Production in Engineered Green Algal Cells* , 2005, Journal of Biological Chemistry.

[59]  Mi‐Sun Kim,et al.  Molecular hydrogen production by nitrogenase of Rhodobacter sphaeroides and by Fe-only hydrogenase of Rhodospirillum rubrum , 2008 .

[61]  M. Tredici,et al.  From open ponds to vertical alveolar panels: the Italian experience in the development of reactors for the mass cultivation of phototrophic microorganisms , 1992, Journal of Applied Phycology.

[62]  R. Telling,et al.  Large-Scale Cultivation of Mammalian Cells , 1970 .

[63]  Frank W. R. Chaplen,et al.  Optimization of media nutrient composition for increased photofermentative hydrogen production by Synechocystis sp. PCC 6803 , 2008 .

[64]  E. Phlips,et al.  Role of Light Intensity and Temperature in the Regulation of Hydrogen Photoproduction by the Marine Cyanobacterium Oscillatoria sp. Strain Miami BG7 , 1983, Applied and environmental microbiology.

[65]  F. G. Acién,et al.  Tubular photobioreactor design for algal cultures. , 2001, Journal of biotechnology.

[66]  René H. Wijffels,et al.  A pneumatically agitated flat-panel photobioreactor with gas re-circulation: anaerobic photoheterotrophic cultivation of a purple non-sulfur bacterium , 2002 .

[67]  L. Stal,et al.  Simultaneous heterolactic and acetate fermentation in the marine cyanobacterium Oscillatoria limosa incubated anaerobically in the dark , 1989, Archives of Microbiology.

[68]  M. Ghirardi,et al.  Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. , 2003, European journal of biochemistry.

[69]  D. Das,et al.  Photofermentative hydrogen production using purple non-sulfur bacteria Rhodobacter sphaeroides O.U.001 in an annular photobioreactor: A case study , 2009 .

[70]  A. Grossman,et al.  The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. , 1998, Plant physiology.

[71]  C. Spruit Simultaneous photoproduction of hydrogen and oxygen by Chlorella , 1958 .

[72]  A. Newton,et al.  SulP, a nuclear gene encoding a putative chloroplast-targeted sulfate permease in Chlamydomonas reinhardtii , 2003, Planta.

[73]  A. Jagendorf,et al.  Photosynthetic Mechanisms of Green Plants , 1964 .

[74]  Jianguo Liu,et al.  Light energy conversion into H2 by Anabaena variabilis mutant PK84 dense cultures exposed to nitrogen limitations , 2006 .

[75]  Y. Asada,et al.  Enhanced hydrogen production by a mutant of Rhodobacter sphaeroides having an altered light-harvesting system. , 1999, Journal of bioscience and bioengineering.

[76]  Yuan-Kun Lee,et al.  Design and performance of an α-type tubular photobioreactor for mass cultivation of microalgae , 1995, Journal of Applied Phycology.

[77]  K. Niyogi,et al.  A Major Light-Harvesting Polypeptide of Photosystem II Functions in Thermal Dissipation Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002154. , 2002, The Plant Cell Online.

[78]  Ghasem D. Najafpour,et al.  Biological hydrogen production from CO: Bioreactor performance , 2008 .

[79]  J. C. Goldman,et al.  Inorganic carbon sources and biomass regulation in intensive microalgal cultures , 1981 .

[80]  V. Belle,et al.  Hyperthermostable and oxygen resistant hydrogenases from a hyperthermophilic bacterium Aquifex aeolicus: Physicochemical properties , 2005 .

[81]  A. Kaminski,et al.  Differential regulation of the Fe-hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. , 2002, European journal of biochemistry.

[82]  L. Rodolfi,et al.  Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low‐cost photobioreactor , 2009, Biotechnology and bioengineering.

[83]  Peter Lindblad,et al.  BioCO2 - a multidisciplinary, biological approach using solar energy to capture CO2 while producing H2 and high value products. , 2007, Biomolecular engineering.

[84]  M. Gibbs,et al.  Fermentative Metabolism of Chlamydomonas reinhardtii: I. Analysis of Fermentative Products from Starch in Dark and Light. , 1984, Plant physiology.

[85]  B. Zabut,et al.  Photoproduction of Hydrogen by rhodobacter sphaeroides O.U.001 in a columan photoreactor: effect of halobacterium halobium , 2015 .

[86]  Wei Zhang,et al.  Two-stage photo-biological production of hydrogen by marine green alga Platymonas subcordiformis , 2004 .

[87]  Jack Legrand,et al.  Investigation of H2 production using the green microalga Chlamydomonas reinhardtii in a fully controlled photobioreactor fitted with on-line gas analysis , 2008 .

[88]  Masahito Taya,et al.  Carbon dioxide fixation in batch culture of Chlorella sp. using a photobioreactor with a sunlight-cellection device , 1996 .

[89]  Mi-Sun Kim,et al.  Photoproduction of hydrogen from acetate by a chemoheterotrophic bacterium Rhodopseudomonas palustris P4 , 2004 .

[90]  The challenge confronting industrial microagriculture: high photosynthetic efficiency in large-scale reactors , 1987 .

[91]  G. Rákhely,et al.  Transposon Mutagenesis in Purple Sulfur Photosynthetic Bacteria: Identification of hypF, Encoding a Protein Capable of Processing [NiFe] Hydrogenases in α, β, and γ Subdivisions of the Proteobacteria , 2001, Applied and Environmental Microbiology.

[92]  K. Miyamoto,et al.  Hydrogen evolution as a consumption mode of reducing equivalents in green algal fermentation. , 1987, Plant physiology.

[93]  Yuan-Kun Lee Enclosed bioreactors for the mass cultivation of photosynthetic microorganisms: the future trend , 1986 .

[94]  P. Vignais,et al.  Occurrence, classification, and biological function of hydrogenases: an overview. , 2007, Chemical reviews.

[95]  Y. Chisti,et al.  Airlift-driven external-loop tubular photobioreactors for outdoor production of microalgae: assessment of design and performance , 2001 .

[96]  Y. Chisti,et al.  Comparative evaluation of compact photobioreactors for large-scale monoculture of microalgae , 1999 .

[97]  Hu Qiang,et al.  Productivity and photosynthetic efficiency ofSpirulina platensis as affected by light intensity, algal density and rate of mixing in a flat plate photobioreactor , 2004, Journal of Applied Phycology.

[98]  I. Eroglu,et al.  Hydrogen production by Rhodobacter sphaeroides O.U.001 in a flat plate solar bioreactor , 2008 .

[99]  Lemi Türker,et al.  Photoproduction of hydrogen from sugar refinery wastewater by Rhodobacter sphaeroides O.U. 001 , 2000 .

[100]  A. Hemschemeier,et al.  A novel screening protocol for the isolation of hydrogen producing Chlamydomonas reinhardtii strains , 2008, BMC Plant Biology.

[101]  Y. Asada,et al.  Photobiological hydrogen production. , 1999, Journal of bioscience and bioengineering.

[102]  Michael Seibert,et al.  Demonstration of sustained hydrogen photoproduction by immobilized, sulfur-deprived Chlamydomonas reinhardtii cells , 2006 .

[103]  Geoffrey D. Smith,et al.  Hydrogen formation by marine blue—green algae , 1977, FEBS letters.

[104]  Juergen E. W. Polle,et al.  tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size , 2003, Planta.

[105]  M. Azuma,et al.  Production of hydrogen by a hydrogenase-deficient mutant of Rhodobacter capsulatus , 1998 .

[106]  Cylindrical-Type Induced and Diffused Photobioreactor , 1998 .

[107]  Clemens Posten,et al.  Closed photo-bioreactors as tools for biofuel production. , 2009, Current opinion in biotechnology.

[108]  G. C. Zittelli,et al.  A vertical alveolar panel (VAP) for outdoor mass cultivation of microalgae and cyanobacteria , 1991 .

[109]  Paula Tamagnini,et al.  Cyanobacterial hydrogenases: diversity, regulation and applications. , 2007, FEMS microbiology reviews.

[110]  F. Martínez-Jerónimo,et al.  A laboratory-scale system for mass culture of freshwater microalgae in polyethylene bags , 1994, Journal of Applied Phycology.

[111]  Ruiyan Zhu,et al.  Hydrogen production by draTGB hupL double mutant of Rhodospirillum rubrum under different light conditions , 2006 .

[112]  E. Grima,et al.  Prediction of dissolved oxygen and carbon dioxide concentration profiles in tubular photobioreactors for microalgal culture , 1999, Biotechnology and bioengineering.

[113]  A. Carvalho,et al.  Microalgal Reactors: A Review of Enclosed System Designs and Performances , 2006, Biotechnology progress.

[114]  John R. Benemann,et al.  Biofuels from Microalgae: Review of Products, Processes and Potential, with Special Focus on Dunaliella sp. , 2009, The Alga Dunaliella.

[115]  G. Codd,et al.  The Uptake and Production of Molecular Hydrogen by Unicellular Cyanobacteria , 1985 .

[116]  Fouchard Swanny,et al.  Investigation of H2 production by microalgae in a fully-controlled photobioreactor , 2006 .

[117]  Ami Ben-Amotz,et al.  The alga Dunaliella : biodiversity, physiology, genomics and biotechnology , 2009 .

[118]  M. Ghirardi,et al.  Microalgae: a green source of renewable H(2). , 2000, Trends in biotechnology.

[119]  Shigeru Uchiyama,et al.  Hydrogen Production by a Floating-Type Photobioreactor , 1998 .

[120]  A. Melis,et al.  Green alga hydrogen production: progress, challenges and prospects , 2002 .

[121]  A. Richmond,et al.  Microalgal biotechnology at the turn of the millennium: A personal view , 2000, Journal of Applied Phycology.

[122]  H2-Uptake and evolution in the unicellular cyanobacterium Chroococcidiopsis thermalis CALU 758 , 2000 .

[123]  D. Hall,et al.  AN AUTOMATED HELICAL PHOTOBIOREACTOR INCORPORATING CYANOBACTERIA FOR CONTINUOUS HYDROGEN PRODUCTION , 1998 .

[124]  Olaf Kruse,et al.  Photosynthetic biomass and H2 production by green algae: from bioengineering to bioreactor scale-up. , 2007, Physiologia plantarum.

[125]  D. Rees,et al.  Structural Basis of Biological Nitrogen Fixation. , 1996, Chemical reviews.

[126]  Gregory Burgess,et al.  Materials, operational energy inputs, and net energy ratio for photobiological hydrogen production , 2007 .

[127]  A. Melis Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae) , 2007, Planta.

[128]  I. Ohad,et al.  Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[129]  Michael W. Fowler,et al.  A flat-sided photobioreactor for culturing microalgae , 1993 .

[130]  Lu Zhang,et al.  Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. , 2000, Plant physiology.

[131]  Spiros N. Agathos,et al.  Study of hydrogen production by three strains of Chlorella isolated from the soil in the Algerian Sahara , 2009 .