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Journal of Applied Phycology

, Volume 27, Issue 4, pp 1415–1423 | Cite as

Effect of nitrogen source and acclimatization on specific growth rates of microalgae determined by a high-throughput in vivo microplate autofluorescence method

  • Michael Podevin
  • Davide De Francisci
  • Susan L. Holdt
  • Irini AngelidakiEmail author
Article

Abstract

Specific growth rates (SGR) of freshwater algae species (Chlorella vulgaris, Auxenochlorella protothecoides, and Chlorella sorokiniana) and the marine species Nannochloropsis oculata on various nitrogen sources (ammonium carbonate, ammonium chloride, sodium nitrate, and urea) could be determined by in vivo chlorophyll-a autofluorescence. These preferences could be determined before large pH changes occurred in the media, with no significant difference (P > 0.05) between buffered and non-buffered media. In all algal species, acclimatization was observed with no significant difference (P > 0.05) between SGRs of the second and third cultivations. ANOVA of SGRs in the acclimatized second and third cultivations revealed preferences for nitrogen sources among most of the algae; C. vulgaris preferred sodium nitrate over other nitrogen sources, A. protothecoides adapted to urea after no growth in the first cultivation, and the SGRs of N. oculata showed an aversion for sodium nitrate over other nitrogen sources (P < 0.05).

Keywords

Adaptation Auxenochlorella Chlorella Nannochloropsis pH changes Industrial wastewater 

Notes

Acknowledgments

This work was funded by the European Commission (EC) Economically and Ecologically Efficient Water Management in the European Chemical Industry (E4Water) project (grant agreement no.: 280756).

References

  1. Bates SS (1976) Effects of light and ammonium on nitrate uptake by two species of estuarine phytoplankton. Limnol Oceanog 21:212–218CrossRefGoogle Scholar
  2. Blaise C, Vasseur P (2005) Algal microplate toxicity test. In: Blaise C, Vasseur P (eds) Small-scale freshwater toxicity investigations. Springer, Berlin, pp 137–179CrossRefGoogle Scholar
  3. Caperon J, Ziemann DA (1976) Synergistic effects of nitrate and ammonium ion on the growth and uptake kinetics of Monochrysis lutheri in continuous culture. Mar Biol 36:73–84CrossRefGoogle Scholar
  4. Davis EA, Dedrick J, French CS, Milner HW, Myers J, Smith JHC, Spoehr HA (1953) Laboratory experiments on Chlorella culture at the Carnegie Institution of Washington Department of Plant Biology. In: Burlew JS (ed) Algal culture from laboratory to pilot plant. Carnegie Institution of Washington Publication no. 600. Carnegie Institution, Washington DC, pp 105–153Google Scholar
  5. Dortch Q (1982) Effect of growth conditions on accumulation of internal nitrate, ammonium, amino acids and protein in three marine diatoms. J Exp Mar Bio Ecol 61:243–264CrossRefGoogle Scholar
  6. Dortch Q (1990) The interaction between nitrate and ammonium uptake in phytoplankton. Mar Ecol Prog Ser 61:183–201CrossRefGoogle Scholar
  7. Dortch Q, Conway H (1984) Interactions between nitrate and ammonium uptake: variation with growth rate, nitrogen source and species. Mar Biol 79:51–164CrossRefGoogle Scholar
  8. Eisentraeger A, Dott W, Klein J, Hahn S (2003) Comparative studies on algal toxicity testing using fluorometric microplate and Erlenmeyer flask growth-inhibition assays. Ecotoxicol Environ Saf 54:346–354PubMedCrossRefGoogle Scholar
  9. Flynn JK, Michael JR, Hipkin F, Hipkin CR (1997) Modeling the interactions between ammonium and nitrate uptake in marine phytoplankton. Phil Trans R Soc B 352:1625–1645PubMedCentralCrossRefGoogle Scholar
  10. Grobbelaar JU (2004) Algal nutrition: mineral nutrition. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science, Oxford, p 104Google Scholar
  11. Guilard RR, Lorenzen C (1972) Yellow-green algae with chlorophyllide. J Phycol 8:10–14Google Scholar
  12. Guillard RR (1975) Culture of phytoplankton for feeding marine invertebrates. In: Guillard RR (ed) Culture of marine invertebrate animals. Springer, Berlin, pp 29–60CrossRefGoogle Scholar
  13. Harisson PT, Berges JA (2005) Marine culture media. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, Burlington, pp 21–34Google Scholar
  14. Hodson RC, Thompson JF (1969) Metabolism of urea by Chlorella vulgaris. Plant Physiol 44:691–696PubMedCentralPubMedCrossRefGoogle Scholar
  15. Hyenstrand P, Burkert U, Pettersson A, Blomqvist P (2000) Competition between the green alga Scenedesmus and the cyanobacterium Synechococcus under different modes of inorganic nitrogen supply. Hydrobiologia 435:91–98CrossRefGoogle Scholar
  16. Hildebrand M (2005) Cloning and functional characterization of ammonium transporters from the marine diatom Cylindrotheca fusiformis (Bacillariophyceae). J Phycol 41:105e113. doi: 10.1111/j.1529-8817.2005.04108.x
  17. Kudela RM, Cochlan WP (2000) Nitrogen and carbon uptake kinetics and the influence of irradiance for a red tide bloom off southern California. Aquat Microb Ecol 21:31–47CrossRefGoogle Scholar
  18. L’Helguen S, Maguer JF, Caradec J (2008) Inhibition kinetics of nitrate uptake by ammonium in size-fractionated oceanic phytoplankton communities: implications for new production and F-ratio estimates. J Plankton Res 30:1179–1188CrossRefGoogle Scholar
  19. MacIntyre HL, Cullen JJ (2005) Measuring growth rates in microalgal cultures. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, Burlington, p 307Google Scholar
  20. Maguer J-F, L’Helguen S, Madec C et al (2007) Nitrogen uptake and assimilation kinetics in Alexandrium minutum (Dinophyceae): effect of N-limited growth rate on nitrate and ammonium interactions. J Phycol 43:295–303CrossRefGoogle Scholar
  21. Mayer P, Cuhel R, Nyholm N (1997) A simple in vitro fluorescence method for biomass measurements in algal growth inhibition tests. Water Res 31:2525–2531CrossRefGoogle Scholar
  22. Needoba JA, Harrison PJ (2004) Influence of low light and a light: dark cycle on NO3 uptake, intracellular NO3 , and nitrogen isotope fractionation by marine phytoplankton. J Phycol 40:505–516CrossRefGoogle Scholar
  23. Peccia J, Haznedaroglu B, Gutierrez J, Zimmerman JB (2013) Nitrogen supply is an important driver of sustainable microalgae biofuel production. Trends Biotechnol 31:134–138PubMedCrossRefGoogle Scholar
  24. Perez-Garcia O, Escalante FM, De-Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36PubMedCrossRefGoogle Scholar
  25. Rebolloso-Fuentes MM, Navarro-Perez A, Garcia-Camacho F, Ramos-Miras JJ, Guil-Guerrero JL (2001) Biomass nutrient profiles of the microalga Nannochloropsis. J Agr Food Chem 49:2966–2972CrossRefGoogle Scholar
  26. Sharma R, Singh GP, Sharma VK (2012) Effects of culture conditions on growth and biochemical profile of Chlorella vulgaris. J Plant Pathol Microbiol 3:1–6CrossRefGoogle Scholar
  27. Shen Y, Yuan W, Pei Z, Mao E (2010) Heterotrophic culture of Chlorella protothecoides in various nitrogen sources for lipid production. Appl Biochem Biotechnol 160:1674–1684PubMedCrossRefGoogle Scholar
  28. Shi X, Zhang X, Chen F (2000) Heterotrophic production of biomass and lutein by Chlorella protothecoides on various nitrogen sources. Enzym Microb Tech 27:312–318CrossRefGoogle Scholar
  29. Shihira I, Krauss RW (1965) Chlorella: physiology and taxonomy of forty-one isolates. University of Maryland College Park, Maryland, pp 1–97Google Scholar
  30. Solomon CM, Glibert PM (2008) Urease activity in five phytoplankton species. Aquatic Microb Ecol 52:149CrossRefGoogle Scholar
  31. Sorokin C (1959) Tabular comparative data for the low-temperature and high-temperature strains of Chlorella. Nature 184:613–614PubMedCrossRefGoogle Scholar
  32. Sturm BS, Lamer SL (2011) An energy evaluation of coupling nutrient removal from wastewater with algal biomass production. Appl Energy 88:3499–3506CrossRefGoogle Scholar
  33. Sunda WG, Price NM, Morel FMM (2005) Trace metal ion buffers and their use in culture studies. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, Burlington, pp 65–82Google Scholar
  34. Syrett PJ, Morris I (1963) The inhibition of nitrate assimilation by ammonium in Chlorella. Biochim Biophys Acta 67:566–575CrossRefGoogle Scholar
  35. Terry KL (1982) Nitrate uptake and assimilation in Thalassiosira weissflogii and Phaeodactylum tricornutum: interactions with photosynthesis and with uptake of other ions. Mar Biol 69:21–30CrossRefGoogle Scholar
  36. USEPA (2010) Inventory of U.S. greenhouse gas emissions and sinks: 1990–2008. (http://www.epa.gov/climatechange/emissions/usinventoryreport.html)
  37. Wood AM, Everroad RC, Wingard LM (2005) Measuring growth rates in microalgal cultures. In: Andersen RA (ed) Algal culturing techniques. Elsevier Academic Press, Burlington, pp 269–285Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Michael Podevin
    • 1
  • Davide De Francisci
    • 1
  • Susan L. Holdt
    • 1
  • Irini Angelidaki
    • 1
    Email author
  1. 1.Department of Environmental EngineeringTechnical University of DenmarkKgs. LyngbyDenmark

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