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Nitrogen Limitation in Neochloris oleoabundans: A Reassessment of Its Effect on Cell Growth and Biochemical Composition

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Abstract

The aim of this work was to reassess the effect of nitrogen limitation (from 0 to 1 mM nitrate), on the growth and the biochemical composition of Neochloris oleoabundans cultures, where only the CO2 available in the air was provided. Slight differences in the initial nitrate concentration, even minimal increments of 0.2 mM, significantly modify the microalgal response towards nitrogen limitation. This stress condition reduced cell proliferation, but increased cell mass values due to the simultaneous accumulation of two storage compounds: lipids, which contained up to a 55.9 % of total fatty acids; and carbohydrates, which may be primarily composed by starch. The highest biomass and lipid productivities of 98.24 and 43.24 mg/l/day, respectively, were attained at an initial nitrate concentration of 0.6 mM. The theoretical annual projection, based on these productivities, allowed the estimation of the liquid fuel energy yields, which are comparable or even higher than those calculated for several biomass feedstocks such as corn, oil palm, sugarcane, or even fast growing grasses, confirming the potential of nitrogen-limited N. oleoabundans biomass as an appropriate feedstock for biofuel purposes.

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References

  1. Chisti, Y. (2007). Biotechnology Advances, 25, 294–306.

    Article  CAS  Google Scholar 

  2. Mata, T. M., Martins, A. A., & Caetano, N. S. (2010). Renewable & Sustainable Energy Reviews, 14, 217–232.

    Article  CAS  Google Scholar 

  3. Meng, X., Yang, J., Xu, X., Zhang, L., Nie, Q., & Xian, M. (2009). Renewable energy, 34, 1–5.

    Article  Google Scholar 

  4. Schenk, P., Thomas-Hall, S., Stephens, E., Marx, U., Mussgnug, J., Posten, C., et al. (2008). Bioenergy Research, 1, 20–43.

    Article  Google Scholar 

  5. Hu, Q., Sommerfeld, M., Jarvis, E., Ghirardi, M., Posewitz, M., Seibert, M., et al. (2008). Plant Journal, 54, 621–639.

    Article  CAS  Google Scholar 

  6. Gerbens-Leenes, W., Hoekstra, A. Y., & van der Meer, T. H. (2009). PNAS, 106, 10219–10223.

    Article  CAS  Google Scholar 

  7. Yang, J., Xu, M., Zhang, X., Hu, Q., Sommerfeld, M., & Chen, Y. (2011). Bioresource Technology, 102, 159–165.

    Article  CAS  Google Scholar 

  8. Band, C. J., Arredondo-Vega, B. O., Vazquez-Duhalt, R., & Greppin, H. (1992). Plant, Cell & Environment, 15, 129–133.

    Article  CAS  Google Scholar 

  9. Sheehan, J., Dunahay, T., Benemman, J. and Roessler, P. (1998), A look back at the U.S. Department of Energy’s Aquatic Species Program — Biodiesel from algae, National Renewable Energy Laboratory, Golden, CO.

  10. Richmond, A. (2004). Handbook of microalgal culture: biotechnology and applied phycology (1st ed.). Oxford: Blackwell Science.

    Google Scholar 

  11. Tornabene, T. G., Holzer, G., Lien, S., & Burris, N. (1983). Enzyme and Microbial Technology, 5, 435–440.

    Article  CAS  Google Scholar 

  12. Gouveia, L., Marques, A., da Silva, T., & Reis, A. (2009). Journal of Industrial Microbiology and Biotechnology, 36, 821–826.

    Article  CAS  Google Scholar 

  13. Yang, Y., Xu, J., Vail, D., & Weathers, P. (2011). Bioresource Technology, 102, 5076–5082.

    Article  CAS  Google Scholar 

  14. Santos, A. M., Janssen, M., Lamers, P. P., Evers, W. A. C., & Wijffels, R. H. (2012). Bioresource Technology, 104, 593–599.

    Article  CAS  Google Scholar 

  15. Arredondo-Vega, B. O., Band, C. J., & Vazquez-Duhalt, R. (1995). Cytobios, 83, 201–205.

    CAS  Google Scholar 

  16. Breuer, G., Lamers, P. P., Martens, D. E., Draaisma, R. B., & Wijffels, R. H. (2012). Bioresource Technology, 124, 217–226.

    Article  CAS  Google Scholar 

  17. Levine, R. B., Costanza-Robinson, M. S., & Spatafora, G. A. (2011). Biomass and Bioenergy, 35, 40–49.

    Article  CAS  Google Scholar 

  18. Li, Y., Horsman, M., Wang, B., Wu, N., & Lan, C. (2008). Applied Microbiology and Biotechnology, 81, 629–636.

    Article  CAS  Google Scholar 

  19. Popovich, C. A., Damiani, C., Constenla, D., Martínez, A. M., Freije, H., Giovanardi, M., et al. (2012). Bioresource Technology, 114, 287–293.

    Article  CAS  Google Scholar 

  20. Pruvost, J., Van Vooren, G., Cogne, G., & Legrand, J. (2009). Bioresource Technology, 100, 5988–5995.

    Article  CAS  Google Scholar 

  21. Knothe, G. (2008). Energy & Fuels, 22, 1358–1364.

    Article  CAS  Google Scholar 

  22. Giovanardi, M., Ferroni, L., Baldisserotto, C., Tedeschi, P., Maietti, A., Pantaleoni, L. and Pancaldi, S. (2013) Protoplasma, 161–174.

  23. Wang, B., & Lan, C. Q. (2011). Bioresource Technology, 102, 5639–5644.

    Article  CAS  Google Scholar 

  24. Wu, N., Li, Y., & Lan, C. (2011). Journal of Polymers and the Environment, 19, 935–942.

    Article  CAS  Google Scholar 

  25. Vazquez-Duhalt, R., & Greppin, H. (1987). Phytochemistry, 26, 885–889.

    Article  CAS  Google Scholar 

  26. Kates, M. (1986). Techniques of lipidology: isolation, analysis and identification of lipids (2nd ed.). Amsterdam: Elsevier.

    Google Scholar 

  27. Thermo Scientific Pierce GC and HPLC technical handbook 2008. Available from: www.fisher.co.uk/techzone/pdfs/pierce/1601383_GChandbook2008.pdf. Accessed October, 2008.

  28. Lowry, O. H., Rosebrough, N. J., Farr, A. L., & Randall, R. J. (1951). Journal of Biological Chemistry, 193, 265–275.

    CAS  Google Scholar 

  29. Chaplin, M. F. (1986). In M. F. Chaplin & J. F. Kennedy (Eds.), Monosaccharides (pp. 1–7). Oxford: IRL Press.

    Google Scholar 

  30. Brewer, P. G., & Goldman, J. C. (1976). Limnology and Oceanography, 21, 108–117.

    Article  CAS  Google Scholar 

  31. Goldman, J. C., Dennett, M. R., & Riley, C. B. (1982). Biotechnology and Bioengineering, 24, 619–631.

    Article  CAS  Google Scholar 

  32. Grossman, A., & Takahashi, H. (2001). Annual Review of Plant Physiology and Plant Molecular Biology, 52, 163–210.

    Article  CAS  Google Scholar 

  33. Piorreck, M., Baasch, K.-H., & Pohl, P. (1984). Phytochemistry, 23, 207–216.

    Article  CAS  Google Scholar 

  34. Courchesne, N. M. D., Parisien, A., Wang, B., & Lan, C. Q. (2009). Journal of Biotechnology, 141, 31–41.

    Article  CAS  Google Scholar 

  35. Thompson, G. A. (1996). Biochimica et Biophysica Acta, 1302, 17–45.

    Article  Google Scholar 

  36. Becker, E. W. (1994). Microalgae: biotechnology and microbiology (1st ed.). Cambridge: Cambridge University Press.

    Google Scholar 

  37. Sanchez Miron, A., Ceron Garcia, M.-C., Garcia Camacho, F., Molina Grima, E., & Chisti, Y. (2002). Enzyme and Microbial Technology, 31, 1015–1023.

    Article  CAS  Google Scholar 

  38. Pruvost, J., Van Vooren, G., Le Gouic, B., Couzinet-Mossion, A., & Legrand, J. (2011). Bioresource Technology, 102, 150–158.

    Article  CAS  Google Scholar 

  39. Rodolfi, L., Chini Zittelli, G., Bassi, N., Padovani, G., Biondi, N., Bonini, G., et al. (2009). Biotechnology and Bioengineering, 102, 100–112.

    Article  CAS  Google Scholar 

  40. Li, Y., Han, D., Sommerfeld, M., & Hu, Q. (2011). Bioresource Technology, 102, 123–129.

    Article  CAS  Google Scholar 

  41. Utting, S. D. (1985). Aquacultural Engineering, 4, 175–190.

    Article  Google Scholar 

  42. Gatenby, C. M., Orcutt, D. M., Kreeger, D. A., Parker, B. C., Jones, V. A., & Neves, R. J. (2003). Journal of Applied Phycology, 15, 1–11.

    Article  CAS  Google Scholar 

  43. Carvalheiro, F., Duarte, L. C., & Gírio, F. M. (2008). Journal of Scientific and Industrial Research, 67, 849–864.

    CAS  Google Scholar 

  44. Lin, Y., & Tanaka, S. (2006). Applied Microbiology and Biotechnology, 69, 627–642.

    Article  CAS  Google Scholar 

  45. Knothe, G. (2005). Fuel Processing Technology, 86, 1059–1070.

    Article  CAS  Google Scholar 

  46. Murray, K. E., Shields, J. A., Garcia, N. D., & Healy, F. G. (2012). Bioresource Technology, 114, 499–506.

    Article  CAS  Google Scholar 

  47. Ma, J. and Hemmers, O. (2010), ASME Conference Proceedings, Phoenix, AZ.

  48. Illman, A. M., Scragg, A. H., & Shales, S. W. (2000). Enzyme and Microbial Technology, 27, 631–635.

    Article  CAS  Google Scholar 

  49. Demirbas, A. (2007). Progress in Energy and Combustion Science, 33, 1–18.

    Article  CAS  Google Scholar 

  50. Naik, S. N., Goud, V. V., Rout, P. K., & Dalai, A. K. (2010). Renewable & Sustainable Energy Reviews, 14, 578–597.

    Article  CAS  Google Scholar 

  51. Demirbas, A. (2011). Applied Energy, 88, 17–28.

    Article  CAS  Google Scholar 

  52. Ohlrogge, J., & Chapman, K. (2011). The Biochemist, 33, 34–38.

    Google Scholar 

  53. US Department of Agriculture, Feed Grains Database. Available from: http://www.ers.usda.gov/data-products/feed-grains-database/feed-grains-custom-query.aspx. Accessed February 22, 2013.

  54. Sheehan, J., Aden, A., Paustian, K., Killian, K., Brenner, J., Walsh, M., et al. (2003). Journal of Industrial Ecology, 7, 117–146.

    Article  CAS  Google Scholar 

  55. US Department of Energy, Theoretical Ethanol Yield Calculator 2006. Available from: http://www1.eere.energy.gov/biomass/ethanol_yield_calculator.html?m=1&. Accessed February 22, 2013.

  56. Martinez-Jimenez, A., Rodriguez-Alegria, M. E., Lopez-Munguia, A., & Gosset-Lagarda, G. (2006). Claridades Agropecuarias, 155, 33–39.

    Google Scholar 

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Acknowledgments

We thank the technical assistance during the project to Mario A. Caro-Bermudez and Mercedes Enzaldo-Cruz. We thank Adriana M. Longoria-Hernandez for technical support in the GC analysis and Maria R. Trejo-Hernandez for providing us with the standards for the fatty acid profile analysis. Adriana Garibay-Hernández held a scholarship from CONACyT-Mexico (No. 10877). This work was supported by Universidad Nacional Autónoma de México, grant DGAPA/PAPIIT/UNAM IT200312.

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  1. Departamento de Ingeniería Celular y Biocatálisis, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Apdo. Postal 510-3, Cuernavaca, Morelos, 62250, Mexico

    Adriana Garibay-Hernández, Rafael Vazquez-Duhalt, Leobardo Serrano-Carreón & Alfredo Martinez

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  1. Adriana Garibay-Hernández
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  2. Rafael Vazquez-Duhalt
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  3. Leobardo Serrano-Carreón
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  4. Alfredo Martinez
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Correspondence to Alfredo Martinez.

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Garibay-Hernández, A., Vazquez-Duhalt, R., Serrano-Carreón, L. et al. Nitrogen Limitation in Neochloris oleoabundans: A Reassessment of Its Effect on Cell Growth and Biochemical Composition. Appl Biochem Biotechnol 171, 1775–1791 (2013). https://doi.org/10.1007/s12010-013-0454-1

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