Sulfate-reducing bacteria as new microorganisms for biological hydrogen production

Abstract Sulfate-reducing bacteria (SRB) have an extremely high hydrogenase activity and in natural habitats where sulfate is limited, produce hydrogen fermentatively. However, the production of hydrogen by these microorganisms has been poorly explored. In this study we investigated the potential of SRB for H2 production using the model organism Desulfovibrio vulgaris Hildenborough. Among the three substrates tested (lactate, formate and ethanol), the highest H2 production was observed from formate, with 320 mL L−1medium of H2 being produced, while 21 and 5 mL L−1medium were produced from lactate and ethanol, respectively. By optimizing reaction conditions such as initial pH, metal cofactors, substrate concentration and cell load, a production of 560 mL L−1medium of H2 was obtained in an anaerobic stirred tank reactor (ASTR). In addition, a high specific hydrogen production rate (4.2 L g−1dcw d−1; 7 mmol g−1dcw h−1) and 100% efficiency of substrate conversion were achieved. These results demonstrate for the first time the potential of sulfate reducing bacteria for H2 production from formate.

[1]  F. Armstrong,et al.  The difference a Se makes? Oxygen-tolerant hydrogen production by the [NiFeSe]-hydrogenase from Desulfomicrobium baculatum. , 2008, Journal of the American Chemical Society.

[2]  M. Durand,et al.  Hydrogenase Activity Control at Desulfovibrio vulgaris Cell‐Coated Carbon Electrodes: Biochemical and Chemical Factors Influencing the Mediated Bioelectrocatalysis , 2002 .

[3]  D. V. Vich,et al.  Hydrogen production and consumption of organic acids by a phototrophic microbial consortium , 2012 .

[4]  F. Kargı,et al.  Comparison of different mixed cultures for bio-hydrogen production from ground wheat starch by combined dark and light fermentation , 2009, Journal of Industrial Microbiology & Biotechnology.

[5]  L. M. Saraiva,et al.  Selenium Is Involved in Regulation of Periplasmic Hydrogenase Gene Expression in Desulfovibrio vulgaris Hildenborough , 2006, Journal of bacteriology.

[6]  Dipankar Ghosh,et al.  Strategies for improving biological hydrogen production. , 2012, Bioresource technology.

[7]  G. Voordouw,et al.  Effects of Deletion of Genes Encoding Fe-Only Hydrogenase of Desulfovibrio vulgaris Hildenborough on Hydrogen and Lactate Metabolism , 2002, Journal of bacteriology.

[8]  P. Matias,et al.  The three-dimensional structure of [NiFeSe] hydrogenase from Desulfovibrio vulgaris Hildenborough: a hydrogenase without a bridging ligand in the active site in its oxidised, "as-isolated" state. , 2010, Journal of molecular biology.

[9]  C. Soares,et al.  Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview. , 2005, Progress in biophysics and molecular biology.

[10]  G. Voordouw,et al.  Function of formate dehydrogenases in Desulfovibrio vulgaris Hildenborough energy metabolism. , 2013, Microbiology.

[11]  M. Faleiro,et al.  Characterization and activity studies of highly heavy metal resistant sulphate-reducing bacteria to be used in acid mine drainage decontamination. , 2009, Journal of hazardous materials.

[12]  Debabrata Das,et al.  Biohydrogen as a renewable energy resource—Prospects and potentials , 2008 .

[13]  Debabrata Das,et al.  Improvement of fermentative hydrogen production: various approaches , 2004, Applied Microbiology and Biotechnology.

[14]  M. Reis,et al.  Hydrogen metabolism in Desulfovibrio desulfuricans strain New Jersey (NCIMB 8313)--comparative study with D. vulgaris and D. gigas species. , 2002, Anaerobe.

[15]  Jizhong Zhou,et al.  Function of Periplasmic Hydrogenases in the Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough , 2007, Journal of bacteriology.

[16]  A. Stams,et al.  The ecology and biotechnology of sulphate-reducing bacteria , 2008, Nature Reviews Microbiology.

[17]  G. Voordouw Carbon Monoxide Cycling by Desulfovibrio vulgaris Hildenborough , 2002, Journal of bacteriology.

[18]  Dipankar Ghosh,et al.  Advances in fermentative biohydrogen production: the way forward? , 2009, Trends in biotechnology.

[19]  A. Stams,et al.  Analysis of the microbial community of the biocathode of a hydrogen-producing microbial electrolysis cell , 2011, Applied Microbiology and Biotechnology.

[20]  Peter Mullany,et al.  Acquired Antibiotic Resistance Genes: An Overview , 2011, Front. Microbio..

[21]  A. Arkin,et al.  The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris , 2009, Journal of bacteriology.

[22]  J. Lloyd Microbial reduction of metals and radionuclides. , 2003, FEMS microbiology reviews.

[23]  Weiwen Zhang,et al.  Global transcriptomics analysis of the Desulfovibrio vulgaris change from syntrophic growth with Methanosarcina barkeri to sulfidogenic metabolism. , 2010, Microbiology.

[24]  C. Soares,et al.  Nickel–Iron–Selenium Hydrogenases – An Overview , 2011 .

[25]  I. Pereira,et al.  A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea , 2011, Front. Microbio..

[26]  Wei Zhao,et al.  Characteristics of hydrogen evolution and oxidation catalyzed by Desulfovibrio caledoniensis biofilm on pyrolytic graphite electrode , 2011 .

[27]  S. Kang,et al.  Thermodynamics of Formate-Oxidizing Metabolism and Implications for H2 Production , 2012, Applied and Environmental Microbiology.

[28]  Jo‐Shu Chang,et al.  Photo fermentative hydrogen production using dominant components (acetate, lactate, and butyrate) in , 2011 .

[29]  M. Wills,et al.  Hydrogen generation from formic acid and alcohols using homogeneous catalysts. , 2010, Chemical Society reviews.

[30]  Anne-Kristin Kaster,et al.  Methanogenic archaea: ecologically relevant differences in energy conservation , 2008, Nature Reviews Microbiology.

[31]  J. M. Odom,et al.  Hydrogen cycling as a general mechanism for energy coupling in the sulfate‐reducing bacteria, Desulfovibrio sp. , 1981 .

[32]  T. Schmidt,et al.  Carbon Dioxide and Formic Acid - The couple for an environmental-friendly hydrogen storage? , 2010 .

[33]  W. Whitman,et al.  Formate-Dependent H2 Production by the Mesophilic Methanogen Methanococcus maripaludis , 2008, Applied and Environmental Microbiology.

[34]  Etsuko Fujita,et al.  Reversible hydrogen storage using CO2 and a proton-switchable iridium catalyst in aqueous media under mild temperatures and pressures , 2012, Nature Chemistry.

[35]  Jizhong Zhou,et al.  Energy metabolism in Desulfovibrio vulgaris Hildenborough: insights from transcriptome analysis , 2008, Antonie van Leeuwenhoek.

[36]  V. Fernández,et al.  Activation and inactivation of hydrogenase function and the catalytic cycle: spectroelectrochemical studies. , 2007, Chemical reviews.

[37]  C. Rodrigues-Pousada,et al.  Tungsten and Molybdenum Regulation of Formate Dehydrogenase Expression in Desulfovibrio vulgaris Hildenborough , 2011, Journal of bacteriology.

[38]  Yvain Nicolet,et al.  Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. , 2007, Chemical reviews.

[39]  Sun-Shin Cha,et al.  Formate-driven growth coupled with H2 production , 2010, Nature.

[40]  Min-Sik Kim,et al.  H2 production from CO, formate or starch using the hyperthermophilic archaeon, Thermococcusonnurineus , 2011, Biotechnology Letters.

[41]  Patrick C. Hallenbeck,et al.  Fermentative hydrogen production: Principles, progress, and prognosis , 2009 .

[42]  Alfons J. M. Stams,et al.  Electron transfer in syntrophic communities of anaerobic bacteria and archaea , 2009, Nature Reviews Microbiology.

[43]  M. Inui,et al.  Enhanced Hydrogen Production from Formic Acid by Formate Hydrogen Lyase-Overexpressing Escherichia coli Strains , 2005, Applied and Environmental Microbiology.

[44]  F. Aulenta,et al.  Linking bacterial metabolism to graphite cathodes: electrochemical insights into the H(2) -producing capability of Desulfovibrio sp. , 2012, ChemSusChem.

[45]  C. Soares,et al.  Hydrogenases in Desulfovibrio vulgaris Hildenborough: structural and physiologic characterisation of the membrane-bound [NiFeSe] hydrogenase , 2005, JBIC Journal of Biological Inorganic Chemistry.

[46]  Y. Oh,et al.  Sustained hydrogen production from formate using immobilized recombinant Escherichia coli SH5 , 2011 .

[47]  Fred J. Brockman,et al.  Global transcriptomic analysis of Desulfovibrio vulgaris on different electron donors , 2006, Antonie van Leeuwenhoek.

[48]  Alfons J. M. Stams,et al.  Syntrophic Growth on Formate: a New Microbial Niche in Anoxic Environments , 2008, Applied and Environmental Microbiology.

[49]  Guangce Wang,et al.  Hydrogen production by a marine photosynthetic bacterium, Rhodovulum sulfidophilum P5, isolated from a shrimp pond , 2012 .

[50]  R. Ludwig,et al.  Efficient Dehydrogenation of Formic Acid Using an Iron Catalyst , 2011, Science.

[51]  Hyung-Sool Lee,et al.  Biological hydrogen production: prospects and challenges. , 2010, Trends in biotechnology.

[52]  Weiwen Zhang,et al.  Metabolic Flexibility of Sulfate-Reducing Bacteria , 2011, Front. Microbio..

[53]  M. Faleiro,et al.  Performance and bacterial community shifts during bioremediation of acid mine drainage from two Portuguese mines , 2011 .

[54]  K. Hanselmann,et al.  Microbial energetics applied to waste repositories , 1991, Experientia.

[55]  A. Spormann,et al.  Lactate conversion to acetate, CO2 and H2 in cell suspensions of Desulfovibrio vulgaris (Marburg): indications for the involvement of an energy driven reaction , 1988, Archives of Microbiology.

[56]  A. Visser,et al.  Biotechnological treatment of sulfate-rich wastewaters. , 1998 .