Advertisement

Applied Biochemistry and Biotechnology

, Volume 177, Issue 1, pp 105–117 | Cite as

Glucose Synthesis in a Protein-Based Artificial Photosynthesis System

  • Hao Lu
  • Wenqiao YuanEmail author
  • Jack Zhou
  • Parkson Lee-Gau Chong
Article

Abstract

The objective of this study was to understand glucose synthesis of a protein-based artificial photosynthesis system affected by operating conditions, including the concentrations of reactants, reaction temperature, and illumination. Results from non-vesicle-based glyceraldehyde-3-phosphate (GAP) and glucose synthesis showed that the initial concentrations of ribulose-1,5-bisphosphate (RuBP) and adenosine triphosphate (ATP), lighting source, and temperature significantly affected glucose synthesis. Higher initial concentrations of RuBP and ATP significantly enhanced GAP synthesis, which was linearly correlated to glucose synthesis, confirming the proper functions of all catalyzing enzymes in the system. White fluorescent light inhibited artificial photosynthesis and reduced glucose synthesis by 79.2 % compared to in the dark. The reaction temperature of 40 °C was optimum, whereas lower or higher temperature reduced glucose synthesis. Glucose synthesis in the vesicle-based artificial photosynthesis system reconstituted with bacteriorhodopsin, F 0 F 1 ATP synthase, and polydimethylsiloxane-methyloxazoline-polydimethylsiloxane triblock copolymer was successfully demonstrated. This system efficiently utilized light-induced ATP to drive glucose synthesis, and 5.2 μg ml−1 glucose was synthesized in 0.78-ml reaction buffer in 7 h. Light-dependent reactions were found to be the bottleneck of the studied artificial photosynthesis system.

Keywords

Artificial photosynthesis Bacteriorhodopsin Copolymer F0F1 ATP synthase Glucose synthesis 

Notes

Acknowledgments

The authors wish to thank Drs. Masasuke Yoshida (Kyoto Sangyo University, Japan) and Toshiharu Suzuki (Hokkaido University, Japan) for the donation of F 0 F 1 ATP synthase. This work was financially supported by the US National Science Foundation (Award # CMMI-1266338; 1266306; 1300792; CBET-1438025; 1437930; 1437798) and the startup fund of North Carolina State University.

References

  1. 1.
    Peter, M. (2002). Energy production from biomass (part 1): overview of biomass. Bioresource Technology, 83(1), 37–46.CrossRefGoogle Scholar
  2. 2.
    Dennis, D. W., John, P. D., Anastasios, M., & Arthur, R. G. (1998). The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiology, 117(1), 129–139.CrossRefGoogle Scholar
  3. 3.
    Thorsten, E. G., Sabine, A., Karl, H. H., Christian, L., & Rainer, M. (1999). Interactions of chronic to elevated CO2 and O3 levels in the photosynthetic light and dark reactions of European beech (Fagus sylvatica). New Phytologist, 144(1), 95–107.CrossRefGoogle Scholar
  4. 4.
    Daniela, S., Andrew, G. L., & John, E. W. (1999). Molecular architecture of the rotary motor in ATP synthase. Science, 286, 1700–1705.CrossRefGoogle Scholar
  5. 5.
    Yoshida, M., Muneyuki, E., & Hisabori, T. (2001). ATP synthase—a marvelous rotary engine of the cell. Nature Reviews, 2, 669–677.CrossRefGoogle Scholar
  6. 6.
    Elston, T., Wang, H. Y., & Oster, G. (1998). Energy transduction in ATP synthase. Letters to Nature, 391, 510–513.CrossRefGoogle Scholar
  7. 7.
    Wang, H. Y., & Oster, G. (1998). Energy transduction in the F1 motor of ATP synthase. Letters to Nature, 396, 279–282.CrossRefGoogle Scholar
  8. 8.
    Weber, J., & Senior, A. E. (2003). ATP synthesis driven by proton transport in F0F1 ATP synthase. FEBS Letters, 545(1), 61–70.CrossRefGoogle Scholar
  9. 9.
    Exton, J. H. (1972). Gluconeogenesis. Metabolism, 21, 945–990.CrossRefGoogle Scholar
  10. 10.
    Zhang, Y. P., & Huang, W. D. (2012). Constructing the electricity-carbohydrate-hydrogen cycle for a sustainability revolution. Trends in Biotechnology, 30(6), 301–306.CrossRefGoogle Scholar
  11. 11.
    Huang, W. D. (2011). Synthesis of sugar and fixation of CO2 through artificial photosynthesis driving by hydrogen or electricity. Journal of University of Science and Technology of China., 41(5), 459–468.Google Scholar
  12. 12.
    Stoeckenius, W., & Bogomolni, R. A. (1982). Bacteriorhodopsin and related pigments of Halobacteria. Annual Review of Biochemistry, 52, 587–616.CrossRefGoogle Scholar
  13. 13.
    Oesterhelt, D. (1998). The structure and mechanism of the family of retinal proteins from halophilic archaea. Current Opinion in Structure Biology, 8(4), 489–500.CrossRefGoogle Scholar
  14. 14.
    Takematsu, S., Nikolou, M., Bernards, D. A., DeFranco, J., Malliaras, G. G., Matsumoto, K., & Shimoyama, I. (2008). Flexible, organic light-pen input device with integrated display. Sensor and Actuators B: Chemical, 135(1), 122–127.CrossRefGoogle Scholar
  15. 15.
    Hampp, N. (2000). Bacteriorhodopsin as a photochromic retinal protein for optical memories. Chemical Review, 100(5), 1755–1776.CrossRefGoogle Scholar
  16. 16.
    Heyn, M. P., & Dencher, N. A. (1982). Reconstitution of monomeric bacteriorhodopsin into phospholipid vesicles. Enzyme in Enzymology, 88, 31–35.Google Scholar
  17. 17.
    Choi, H. J., Germain, J., & Montemagno, C. D. (2006). Effects of different reconstitution procedures on membrane protein activities in proteopolymersomes. Nanotechnology, 17, 1825–1830.CrossRefGoogle Scholar
  18. 18.
    Choi, H. J., Germain, J., & Montemagno, C. D. (2006). Biosynthesis within a bubble architecture. Nanotechnology, 17, 2198–2202.CrossRefGoogle Scholar
  19. 19.
    Hazard, A., & Montemagno, C. D. (2002). Improved purification for thermophilic F0F1 ATP synthase using n-dodecyl β-D-maltoside. Archives of Biochemistry and Biophysics, 407(1), 117–124.CrossRefGoogle Scholar
  20. 20.
    Ward, D. A., & Keys, A. J. (1989). A comparison between the coupled spectrophotometric and uncoupled radiometric assays for RuBP carboxylase. Photosynthesis Research, 22(2), 167–171.CrossRefGoogle Scholar
  21. 21.
    Pan, X. L., Fan, Z. L., Chen, W., Ding, Y. J., Luo, H. Y., & Bao, X. H. (2007). Enhanced ethanol production inside carbon-nanotube reactors containing catalytic particles. Nature Materials, 6, 507–511.CrossRefGoogle Scholar
  22. 22.
    Laser, M., Schulman, D., Allen, S. G., Lichwa, J., Antal, M. J., & Lynd, L. R. (2002). A comparison of liquid hot water and steam pretreatments of sugarcane bagasse for bioconversion to ethanol. Bioresource Technology, 81(1), 33–44.CrossRefGoogle Scholar
  23. 23.
    Krishnan, C., Sousa, L. C., Jin, M. J., Chang, L. P., Dale, B. E., & Balan, V. (2010). Alkali-Based AFEX pretreatment for the conversion of sugarcane bagasse and cane leaf residues to ethanol. Biotechnology Bioengineering, 107(3), 441–450.CrossRefGoogle Scholar
  24. 24.
    Goldemberg, J., Coelho, S. T., & Guardabassi, P. (2008). The sustainability of ethanol production from sugarcane. Energy Policy, 36(6), 2086–2097.CrossRefGoogle Scholar
  25. 25.
    Wendell, D., Todd, J., & Montemagno, C. D. (2010). Artificial photosynthesis in Ranspumin-2 based foam. Nano Letters, 10(9), 3231–3236.CrossRefGoogle Scholar
  26. 26.
    Seigneuret, M., & Rigaud, J. L. (1985). Use of the fluorescent pH probe pyranine to detect heterogeneous directions of proton movement in bacteriorhodopsin reconstituted large liposomes. Federation of European Biochemical Societies Letters, 188(1), 101–106.CrossRefGoogle Scholar
  27. 27.
    Overly, C. C., Lee, K. D., Berthiaume, E., & Hollenbeck, P. J. (1995). Quantitative measurement of intraorganelle pH in the endosomal-lysosomal pathway in neurons by using ratiometric imaging with pyranine. Neurobioology, 92(8), 3156–3160.Google Scholar
  28. 28.
    Pitard, B., Richard, P., Dunach, M., Girault, G., & Rigaud, J. L. (1996). ATP synthesis by the F0F1 ATP synthase from thermophilic Bacillus PS3 reconstituted into liposomes with bacteriorhodopsin. 1. Factors defining the optimal reconstitution of ATP synthases with bacteriorhodopsin. European Journal of Biochemistry, 235(3), 769–778.CrossRefGoogle Scholar
  29. 29.
    Wong, C. H., & Whitesides, G. M. (1983). Synthesis of sugars by aldolase-catalyzed consendation reactions. Journal of Organic Chemistry, 48(19), 3199–3205.CrossRefGoogle Scholar
  30. 30.
    Powles, S. B. (1984). Photoinhibition of photosynthesis induced by visible light. Annual Review of Plant Physiology, 35, 15–44.CrossRefGoogle Scholar
  31. 31.
    Preiss, J., & Kosuge, T. (1970). Regulation of enzyme activity in photosynthetic systems. Annual Review of Plant Physiology, 21, 433–466.CrossRefGoogle Scholar
  32. 32.
    Portis, A. R. (1992). Regulation of ribulose 1, 5-bisphosphate carboxylase/oxygenase activity. Annual Review of Plant Physiology, 43, 415–437.CrossRefGoogle Scholar
  33. 33.
    Dec, J., & Bollag, J. M. (1990). Detoxification of substituted phenols by oxidoreductive enzymes through polymerization reaction. Archives of Environment Contamination and Toxicology, 19, 543–550.CrossRefGoogle Scholar
  34. 34.
    Wrba, A., Schweiger, A., Schultes, V., & Jaenick, R. (1990). Extremely thermostable glyceraldehyde-3-phosphate dehydrogenase from the eubacterium Thermotoga maritime. Biochemistry, 29(33), 7584–7592.CrossRefGoogle Scholar
  35. 35.
    Thomas, T. M., & Scopes, R. K. (1998). The effects of temperature on the kinetics and stability of mesophilic and thermophilic 3-phosphoglycerate kinases. Biochemical Journal, 330, 1087–1095.CrossRefGoogle Scholar
  36. 36.
    Daniel, M. R., Dines, M., & Petach, H. H. (1996). The denaturation and degradation of stable enzymes at high temperatures. Biochemical Journal, 317, 1–11.CrossRefGoogle Scholar
  37. 37.
    Richard, P., Pitard, B., & Rigaud, J. L. (1995). ATP synthesis by the F0F1-ATPase from the thermophilic Bacillus PS3 coreconstituted with bacteriorhodopsin into liposomes. Journal of Biological Chemistry, 270, 21571–21578.CrossRefGoogle Scholar
  38. 38.
    Choi, H. J., Lee, H., & Montemagno, C. D. (2005). Toward hybrid proteo-polymeric vesicles generating a photoinduced proton gradient for biofuel cells. Nanotechnology, 16(9), 1589–1597.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Hao Lu
    • 1
  • Wenqiao Yuan
    • 1
    Email author
  • Jack Zhou
    • 2
  • Parkson Lee-Gau Chong
    • 3
  1. 1.Department of Biological and Agricultural EngineeringNorth Carolina State UniversityRaleighUSA
  2. 2.Department of Mechanical Engineering and MechanicsDrexel UniversityPhiladelphiaUSA
  3. 3.Department of Medical Genetics and Molecular BiochemistryTemple University School of MedicinePhiladelphiaUSA

Personalised recommendations