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Enhanced dark fermentative H2 production by agar-immobilized cyanobacterium Aphanothece halophytica

  • Sunisa Pansook
  • Aran IncharoensakdiEmail author
  • Saranya PhunpruchEmail author
Article

Abstract

Cell immobilization is one of the techniques used to improve H2 productivity in cyanobacteria. In this study, H2 production by immobilized cells of unicellular halotolerant cyanobacterium Aphanothece halophytica was investigated and optimized. The results showed that immobilized cells of A. halophytica had higher H2 production than free cells under nitrogen-deprived condition. Among various support material types used, agar-immobilized cells showed the highest H2 production rate. Under nitrogen deprivation, the optimal conditions of cell immobilization for H2 production were 3% (w/v) agar concentration, 0.2 mg dry cell weight per mL of gel solution, and 0.125 cm3 of agar cube. The optimum pH of medium and incubation temperature for H2 production by agar-immobilized cells were pH 7.4 and 40 °C, respectively. Using a large glass vial and headspace volume resulted in enhancement of H2 production by agar-immobilized cells. Finally, H2 production by agar-immobilized cells was analyzed for three consecutive cycles. H2 production could be maintained at the highest level after two cycles when half of immobilized cells were replaced with fresh immobilized cells. These findings indicate that the enhanced H2 production of the unicellular halotolerant cyanobacterium A. halophytica can be achieved by immobilization method, thus providing the possibility to improve H2 production by cyanobacteria in the future.

Keywords

H2 production Immobilization Cyanobacteria Aphanothece halophytica 

Notes

Funding information

This study was financially supported by research grant from the Office of the Higher Education Commission under the contract no. 2558A11862004 and also by research grant from Faculty of Science, King Mongkut’s Institute of Technology Ladkrabang. A.I. received research grant from the Thailand Research Fund (IRG5780008).

References

  1. Altimari P, Di Caprio F, Toro L, Capriotti AL, Pagnanelli F (2014) Hydrogen photo-production by mixotrophic cultivation of Chlamydomonas reinhardtii: interaction between organic carbon and nitrogen. Chem Eng Trans 38:199–204Google Scholar
  2. Ananyev G, Carrieri D, Dismukes GC (2008) Optimization of metabolic capacity and flux through environmental cues to maximize hydrogen production by the cyanobacterium “Arthrospira (Spirulina) maxima”. Appl Environ Microbiol 74:6102–6113CrossRefGoogle Scholar
  3. Anjana K, Kaushik A (2014) Enhanced hydrogen production by immobilized cyanobacterium Lyngbya perelegans under varying anaerobic conditions. Biomass Bioenergy 63:54–57CrossRefGoogle Scholar
  4. Babich H, Stotzky G (1983) Toxicity of nickel to microbes: environmental aspects. Adv Appl Microbiol 29:195–265CrossRefGoogle Scholar
  5. Bickerstaff GF (1995) Impact of genetic technology on enzyme technology. Genet Eng Biotechnol 15:13–30Google Scholar
  6. Chen PC, Fan SH, Chiang CL, Lee CM (2008) Effect of growth conditions on the hydrogen production with cyanobacterium Anabaena sp. strain CH3. Int J Hydrog Energy 33:1460–1464CrossRefGoogle Scholar
  7. Freeman A (1984) Gel entrapment of whole cells and enzymes in crosslinked, prepolymerized polyacrylamide hydrazide. Ann N Y Acad Sci 434:418–426CrossRefGoogle Scholar
  8. Garlick S, Oren A, Padan E (1997) Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria. J Bacteriol 129:623–629Google Scholar
  9. Karube I, Ikemoto H, Kajiwara K, Tamiya E, Matsuoka H (1986) Photochemical energy conversion using immobilized blue-green algae. J Biotechnol 4:73–80CrossRefGoogle Scholar
  10. Kotay SM, Das D (2008) Biohydrogen as a renewable energy resource - prospects and potentials. Int J Hydrog Energy 33:258–263CrossRefGoogle Scholar
  11. Kumar S, Subhashini CHT, Polasa H (1991) Photoproduction of molecular hydrogen by an immobilized non-diazotrophic cyanobacterium, Oscillatoria subbrevis strain 111. Proc Indian Natl Sci Acad B57:89–94Google Scholar
  12. Kumazawa S, Mitsui A (1981) Characterization and optimization of hydrogen photoproduction by saltwater blue-green algae, Oscillatoria sp. Miami BG7. I. Enhancement through limiting the supply of nitrogen nutrients. Int J Hydrog Energy 6:339–348CrossRefGoogle Scholar
  13. Kuwada Y, Ohta Y (1989) Hydrogen production and carbohydrate consumption by Lyngbya sp. (No. 108). Agric Biol Chem 53:2847–2851Google Scholar
  14. Leino H, Kosourov SN, Saari L, Sivonen K, Tsygankov AA, Aro EM, Allahverdiyeva Y (2009) Extended H2 photoproduction by N2-fixing cyanobacteria immobilized in thin alginate films. Int J Hydrog Energy 37:151–156CrossRefGoogle Scholar
  15. Lin JT, Stewart V (1997) Nitrate assimilation by bacteria. Adv Microb Physiol 39:1–30CrossRefGoogle Scholar
  16. Nguyen BT, Nicolai T, Benyahia L, Chassenieux C (2014) Synergistic effects of mixed salt on the gelation of κ-carrageenan. Carbohydr Polym 112:10–15CrossRefGoogle Scholar
  17. Pansook S, Incharoensakdi A, Phunpruch S (2016) Hydrogen production by immobilized cells of unicellular halotolerant cyanobacterium Aphanothece halophytica in alginate beads. Asia Pac J Sci Technol 22:248–255Google Scholar
  18. Perry JH (1963) Chemical engineers’ handbook. McGraw-Hill, New YorkGoogle Scholar
  19. Peters JW, Schut GJ, Boyd ES, Mulder DW, Shepard EM, Broderick JB, Adams MW (2015) [FeFe]-and [NiFe]-hydrogenase diversity, mechanism, and maturation. Biochim Biophys Acta-Mol Cell Res 1853:1350–1369CrossRefGoogle Scholar
  20. Phunpruch S, Taikhao S, Incharoensakdi A (2016) Identification of bidirectional hydrogenase genes and their co-transcription in unicellular halotolerant cyanobacterium Aphanothece halophytica. J Appl Phycol 28:967–978CrossRefGoogle Scholar
  21. Rashid N, Song W, Park J, Jin HF, Lee K (2009) Characteristics of hydrogen production by immobilized cyanobacterium Microcystis aeruginosa through cycles of photosynthesis and anaerobic incubation. J Ind Eng Chem 15:498–503CrossRefGoogle Scholar
  22. Reddy PM, Spiller H, Albrecht SL, Shanmugam KT (1996) Photodissimilation of fructose to H2 and CO2 by a dinitrogen-fixing cyanobacterium, Anabaena variabilis. Appl Environ Microbiol 62:1220–1226Google Scholar
  23. Rippka R, Deruelles J, Waterbury J, Herdman M, Stanier R (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61Google Scholar
  24. Sarkar S, Pandey KD, Kashyap AK (1992) Hydrogen photoproduction by filamentous non-heterocystous cyanobacterium Plectonema boryanum and simultaneous release of ammonia. Int J Hydrog Energy 17:689–694CrossRefGoogle Scholar
  25. Scott CL (2012) The use of agar as a solvent gel in objects conservation. Objects Specialty Group Postprints 19:71–83Google Scholar
  26. Semenchuk IN, Taranova LA, Kalenyuk AA, Il’yasov PV, Reshetilov AN (2000) Effect of various methods of immobilization on the stability of a microbial biosensor for surfactants based on Pseudomonas rathonis T. Appl Biochem Microbiol 36:69–72Google Scholar
  27. Seol E, Manimaran A, Jang Y, Kim S, Oh Y-K, Park S (2011) Sustained hydrogen production from formate using immobilized recombinant Escherichia coli SH5. Int J Hydrog Energy 36:8681–8686CrossRefGoogle Scholar
  28. Serebryakova LT, Tsygankov AA (2007) Two-stage system for hydrogen production by immobilized cyanobacterium Gloeocapsa alpicola CALU 743. Biotechnol Prog 23:1106–1110CrossRefGoogle Scholar
  29. Serebryakova LT, Sheremetieva M, Tsygankov AA (1998) Reversible hydrogenase activity of Gloeocapsa alpicola in continuous culture. FEMS Microbiol Lett 166:89–94CrossRefGoogle Scholar
  30. Taikhao S, Phunpruch S (2017) Increasing hydrogen production efficiency of N2-fixing cyanobacterium Anabaena siamensis TISTR 8012 by cell immobilization. Energy Procedia 138:366–371CrossRefGoogle Scholar
  31. Taikhao S, Junyapoon S, Incharoensakdi A, Phunpruch S (2013) Factors affecting biohydrogen production by unicellular halotolerant cyanobacterium Aphanothece halophytica. J Appl Phycol 25:575–585CrossRefGoogle Scholar
  32. Taikhao S, Incharoensakdi A, Phunpruch S (2015) Dark fermentative hydrogen production by the unicellular halotolerant cyanobacterium Aphanothece halophytica grown in seawater. J Appl Phycol 27:187–196CrossRefGoogle Scholar
  33. Takabe T, Incharoensakdi A, Arakawa K, Yokota S (1988) CO2 fixation rate and RuBisCO content increase in the halotolerant cyanobacterium, Aphanothece halophytica, grown in high salinities. Plant Physiol 88:1120–1124CrossRefGoogle Scholar
  34. Tamagnini P, Leitão E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31:692–720CrossRefGoogle Scholar
  35. Touloupakis E, Rontogiannis G, Benavides AMS, Cicchi B, Ghanotakis DF, Torzillo G (2016) Hydrogen production by immobilized Synechocystis sp. PCC 6803. Int J Hydrog Energy 41:15181–15186CrossRefGoogle Scholar
  36. Troshina O, Serebryakova LT, Sheremetieva M, Lindblad P (2002) Production of H2 by the unicellular cyanobacterium Gloeocapsa alpicola CALU743 during fermentation. Int J Hydrog Energy 27:1283–1289CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Biology, Faculty of ScienceKing Mongkut’s Institute of Technology LadkrabangBangkok 10520Thailand
  2. 2.Laboratory of Cyanobacterial Biotechnology, Department of Biochemistry, Faculty of ScienceChulalongkorn UniversityBangkok 10330Thailand
  3. 3.Academy of ScienceRoyal Society of ThailandBangkok 10300Thailand
  4. 4.Bioenergy Research Unit, Faculty of ScienceKing Mongkut’s Institute of Technology LadkrabangBangkok 10520Thailand

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