Skip to main content

Advertisement

SpringerLink
Log in

Hydrogen Generation Through Indirect Biophotolysis in Batch Cultures of the Nonheterocystous Nitrogen-Fixing Cyanobacterium Plectonema boryanum

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The nitrogen-fixing nonheterocystous cyanobacterium Plectonema boryanum was used as a model organism to study hydrogen generation by indirect biophotolysis in nitrogen-limited batch cultures that were continuously illuminated and sparged with argon/CO2 to maintain anaerobiosis. The highest hydrogen-production rate (i.e., 0.18 mL/mg day or 7.3 µmol/mg day) was observed in cultures with an initial medium nitrate concentration of 1 mM at a light intensity of 100 µmol/m2 s. The addition of photosystem II (PSII) inhibitor 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU) did not reduce hydrogen-production rates relative to unchallenged controls for 50 to 150 h, and intracellular glycogen concentrations decreased significantly during the hydrogen generation period. The insensitivity of the hydrogen-production process to DCMU is indicative of the fact that hydrogen was not derived from water splitting at PSII (i.e., direct biophotolysis) but rather from electrons provided by intracellular glycogen reserves (i.e., indirect biophotolysis). It was shown that hydrogen generation could be sustained for long time periods by subjecting the cultures to alternating cycles of aerobic, nitrogen-limited growth and anaerobic hydrogen production.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Huesemann, M. H. (2006). Can advances in science and technology prevent global warming? A critical review of limitations and challenges. Mitigation and Adaptation Strategies for Global Change, 11, 539–577.

    Article  Google Scholar 

  2. Prince, R. C., & Kheshgi, H. S. (2005). The photobiological production of hydrogen: Potential efficiency and effectiveness as a renewable fuel. Critical Reviews in Microbiology, 31, 19–31.

    Article  CAS  Google Scholar 

  3. Healey, F. P. (1970). Hydrogen evolution by several algae. Planta, 91, 220–226.

    Article  CAS  Google Scholar 

  4. Ghirardi, M. L., Zhang, L., Lee, J. W., Flynn, T., Seibert, M., Greenbaum, E., et al. (2000). Microalgae: A green source of renewable H2. Trends in Biotechnology, 18, 506–511.

    Article  CAS  Google Scholar 

  5. Melis, A., & Happe, T. (2001). Hydrogen production: Green algae as a source of energy. Plant Physiology, 127, 740–748.

    Article  CAS  Google Scholar 

  6. Benemann, J. R. (1996). Hydrogen biotechnology: Progress and prospects. Nature Biotechnology, 14, 1101–1103.

    Article  CAS  Google Scholar 

  7. Benemann, J. R. (1997). Feasibility analysis of photobiological hydrogen production. International Journal of Hydrogen Energy, 22(10), 979–987.

    Article  CAS  Google Scholar 

  8. Tredici, M., Zittelli, G., & Benemann, J. R. (1998). In O. Zaborsky, et al. (Eds.), BioHydrogen (pp. 391–402). New York: Plenum.

  9. Hallenbeck, P. C., & Benemann, J. R. (2002). Biological hydrogen production: Fundamentals and limiting processes. International Journal of Hydrogen Energy, 27, 1185–1193.

    Article  CAS  Google Scholar 

  10. Benemann, J. R., & Weare, N. M. (1974). Hydrogen evolution by nitrogen-fixing Anabaena cylindrica cultures. Science, 184, 174–175.

    Article  CAS  Google Scholar 

  11. Kashyak, A. K., Pandey, K. D., & Sarkar, S. (1996). Enhanced hydrogen photoproduction by non-heterocystous cyanobacterium Plectonema boryanum. International Journal of Hydrogen Energy, 21(2), 107–109.

    Article  Google Scholar 

  12. Rogerson, A. C. (1980). Nitrogen fixing growth by non-heterocystous cyanobacterium Plectonema boryanum. Nature, 284, 563–564.

    Article  CAS  Google Scholar 

  13. Weare, N. M., & Benemann, J. R. (1974). Nitrogenase activity and photosynthesis in Plectonema boryanum. Journal of Bacteriology, 119(1), 258–265.

    CAS  Google Scholar 

  14. Burrows, E. H., Chaplen, F. W. R., & Ely, R. L. (2008). Optimization of media nutrient composition for increased photofermentative hydrogen production by Synechocystis sp. PCC 6803. International Journal of Hydrogen Energy, 33(21), 6092–6099.

    Article  CAS  Google Scholar 

  15. Troshina, O., Serebryakova, L., Sheremetieva, M., & Lindblad, P. (2002). Production of hydrogen by the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermentation. International Journal of Hydrogen Energy, 27(11–12), 1283–1289.

    Article  CAS  Google Scholar 

  16. Yoo, S. H., Keppel, C., Spalding, M., & Jane, J. L. (2007). Effects of growth condition on the structure of glycogen produced in cyanobacterium Synechocystis sp. PCC6803. International Journal of Biological Macromolecules, 40(5), 498–504.

    Article  CAS  Google Scholar 

  17. Dutta, D., De, D., Chaudhuri, S., & Bhattacharya, S. K. (2005). Hydrogen production by cyanobacteria. Microbial Cell Factories, 4, 36.

    Article  CAS  Google Scholar 

  18. Madamwar, D., Garg, N., & Shah, V. (2000). Cyanobacterial hydrogen production. World Journal of Microbiology and Biotechnology, 16, 757–767.

    Article  CAS  Google Scholar 

  19. Rao, K. K., & Hall, D. O. (1996). Hydrogen production by cyanobacteria: Potentials, problems, and prospects. Journal of Marine Biotechnology, 4, 10–15.

    CAS  Google Scholar 

  20. Berry, S., Bolychevtseva, Y. V., Rogner, M., & Karapetyan, N. V. (2003). Photosynthetic and respiratory electron transport in the alkaliphilic cyanobacterium Arthrospira (Spirulina) platensis. Photosynthesis Research, 78, 67–76.

    Article  CAS  Google Scholar 

  21. Tett, P., Kelly, M. G., & Hornberger, G. M. (1975). A method for the spectrophotometric measurement of chlorophyll-a and pheophytin a in benthic microalgae. Limnology and Oceanography, 20(5), 887–896.

    Article  Google Scholar 

  22. Gfeller, R., & Gibbs, M. (1984). Fermentative metabolism of Chlamydomonas reinhardtii. Plant Physiology, 7(75), 212–218.

    Article  Google Scholar 

  23. Bergmeyer, H. U., & Bernt, E. (1974). Methods of enzymatic analysis (2nd ed., pp. 1205–1212). New York: Academic.

    Google Scholar 

  24. Pauss, A., Andre, G., Perrier, M., & Guiot, S. R. (1990). Liquid-to-gas mass transfer in anaerobic processes: Inevitable transfer limitations of methane and hydrogen in the biomethanation process. Applied and Environmental Microbiology, 56(6), 1636–1644.

    CAS  Google Scholar 

  25. Huesemann, M. H., Hausmann, T. S., Bartha, R., Aksoay, M., Polle, J., Weissman, J. C., et al. (2009). Biomass productivities in wild type and a new pigment mutant of Cyclotella sp. (Diatom). Applied Biochemistry and Biotechnology, 157(3), 507–526.

    Article  CAS  Google Scholar 

  26. Kumazawa, S., & Mitsui, A. (1981). Characterization and optimization of hydrogen photoproduction by a saltwater blue–green alga, Oscillatoria sp. Miami BG7. 1. Enhancement through limiting the supply of nitrogen nutrients. International Journal of Hydrogen Energy, 6, 339–348.

    Article  CAS  Google Scholar 

  27. Markov, S., Weaver, P. F., & Seibert, M. (1996). Hydrogen production using microorganisms in hollow-fiber bioreactors. In T. N. Verziroglu, et al. (Eds.), Hydrogen energy progress XI, Proceedings of the 11th World Hydrogen Energy Conference, Stuttgart, Germany, 23–28 June 1996, volume 3 (pp. 2619–2624). Frankfurt am Main: Schon and Wetzel.

    Google Scholar 

  28. Ghirardi, M. L., Kosourov, S., Tsygankov, A., & Seibert, M. (2000b). Two-phase photobiological algal H2-production system. Proceedings of the 2000 DOE Hydrogen Program Review, NREL/CP-570-28890.

  29. Kosourov, S., Seibert, M., & Ghirardi, M. L. (2003). Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H2-producing Chlamydomonas reinhardtii cultures. Plant Cell Physiology, 44(2), 146–155.

    Article  CAS  Google Scholar 

  30. Melis, A., Zhang, L., Forestier, M., Ghirardi, M. L., & Seibert, M. (2000). Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green algae Chlamydomonas reinhardtii. Plant Physiology, 122, 127–136.

    Article  CAS  Google Scholar 

  31. Benemann, J. R. (1998). Process analysis and economics of biophotolysis of water. Report to the International Energy Agency (IEA), IEA/H2/10/TR2-98, March 1998.

Download references

Acknowledgements

Funding for this project was provided by the Department of Energy National Energy Technology Laboratory and two SULI stipends from the Department of Energy Office of Science to Blaine Carter and Jared Gerschler, respectively.

Author information

Authors and Affiliations

  1. Marine Sciences Laboratory, Pacific Northwest National Laboratory, 1529 West Sequim Bay Road, Sequim, WA, 98382, USA

    Michael H. Huesemann, Tom S. Hausmann, Blaine M. Carter & Jared J. Gerschler

  2. Benemann Associates, 3434 Tice Creek Drive, #1, Walnut Creek, CA, 94595, USA

    John R. Benemann

Authors
  1. Michael H. Huesemann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tom S. Hausmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Blaine M. Carter
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jared J. Gerschler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. John R. Benemann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael H. Huesemann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huesemann, M.H., Hausmann, T.S., Carter, B.M. et al. Hydrogen Generation Through Indirect Biophotolysis in Batch Cultures of the Nonheterocystous Nitrogen-Fixing Cyanobacterium Plectonema boryanum . Appl Biochem Biotechnol 162, 208–220 (2010). https://doi.org/10.1007/s12010-009-8741-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-009-8741-6

Keywords

Search

Navigation