Advertisement

Journal of Applied Phycology

, Volume 26, Issue 3, pp 1359–1377 | Cite as

Effect of nutrient supply status on biomass composition of eukaryotic green microalgae

  • Gita Procházková
  • Irena Brányiková
  • Vilém Zachleder
  • Tomáš BrányikEmail author
Article

Abstract

In eukaryotic green microalgae, manipulation of metabolic pathways by altering the culture medium and/or culture conditions represents a powerful tool for physiological control and is usually more practicable than metabolic or genetic engineering. Strategies for nutrient-induced shifts in biomass composition are generally cost-efficient, environmentally friendly, applicable on a large scale and flexible for various industrially attractive microalgae species. In addition, processes, such as nutrient limitation/deprivation, can be readily scheduled and optimised to achieve high levels of productivity for the desired target compound(s). These strategies are currently used in microalgae to achieve overproduction of metabolites such as lipids, polysaccharides and pigments. This paper presents an overview of the species and strain-specific responses of eukaryotic, green microalgal cells that are triggered by variations in selected macronutrient and micronutrient availability. Individual and mutually associated physiological responses to nutrient supply status are described at the molecular level as well as discussed from the perspective of potential biotechnological applications.

Keywords

Green microalgae Nutrients Limitation Metabolic response Biomass composition Cell growth 

Notes

Acknowledgment

The authors thank the Czech Grant Agency (P503/10/1270) for financial support.

References

  1. Adams C, Godfrey V, Wahlen B, Seefeldt L, Bugbee B (2013) Understanding precision nitrogen stress to optimize the growth and lipid content tradeoff in oleaginous green microalgae. Bioresour Technol 131:188–194PubMedGoogle Scholar
  2. Antal T, Krendeleva T, Rubin A (2011) Acclimation of green algae to sulfur deficiency: underlying mechanisms and application for hydrogen production. Appl Microbiol Biotechnol 89:3–15PubMedGoogle Scholar
  3. Araie H, Shiraiwa Y (2009) Selenium utilization strategy by microalgae. Molecules 14:4880–4891PubMedGoogle Scholar
  4. Axley MJ, Stadtman TC (1989) Selenium metabolism and selenium-dependent enzymes in microorganisms. Annu Rev Nutr 9:127–137PubMedGoogle Scholar
  5. Badger MR, Kaplan A, Berry JA (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii: evidence for a carbon dioxide-concentrating mechanism. Plant Physiol 66:407–413PubMedCentralPubMedGoogle Scholar
  6. Ballin G, Doucha J, Zachleder V, Šetlík I (1988) Macromolecular syntheses and the course of cell cycle events in the chlorococcal alga Scenedesmus quadricauda under nutrient starvation: effect of nitrogen starvation. Biol Plant 30:81–91Google Scholar
  7. Bannister T (1979) Quantitative description of steady state, nutrient-saturated algal growth, including adaptation. Limnol Oceanogr 24:76–96Google Scholar
  8. Barsanti L, Gualtieri P (2006) Algal culturing. In: Barsanti L, Gualtieri P (eds) Algae: anatomy, biochemistry and biotechnology. CRC Press, Boca Ranton, pp 209–250Google Scholar
  9. Batyrova KA, Tsygankov AA, Kosourov SN (2012) Sustained hydrogen photoproduction by phosphorus-deprived Chlamydomonas reinhardtii cultures. Int J Hydrogen Energy 37:8834–8839Google Scholar
  10. Becker EW (1994) Culture media. In: Becker EW (ed) Microalgae: biotechnology and microbiology. Cambridge University Press, Cambridge, pp 9–41Google Scholar
  11. Ben-Amotz A (1995) New mode of Dunaliella biotechnology: two-phase growth for β-carotene production. J Appl Phycol 7:65–68Google Scholar
  12. Besser JM, Canfield TJ, La Point TW (1993) Bioaccumulation of organic and inorganic selenium in a laboratory food chain. Environ Toxicol Chem 12:57–72Google Scholar
  13. Borowitzka MA (2013) Dunaliella: biology, production, and markets. In: Richmond A, Hu Q (eds) Handbook of microalgal culture. Wiley, pp 359–368Google Scholar
  14. Boussiba S (2000) Carotenogenesis in the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 108:111–117Google Scholar
  15. Brányiková I, Maršálková B, Doucha J, Brányik T, Bišová K, Zachleder V, Vítová M (2011) Microalgae—novel highly efficient starch producers. Biotechnol Bioeng 108:766–776PubMedGoogle Scholar
  16. Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226PubMedGoogle Scholar
  17. Buetow DE (1965) Growth, survival and biochemical alteration of Euglena gracilis in medium limited in sulfur. J Cell Comp Physiol 66:235–242Google Scholar
  18. Burrows EH, Chaplen FWR, Ely RL (2008) Optimization of media nutrient composition for increased photofermentative hydrogen production by Synechocystis sp. PCC 6803. Int J Hydrogen Energy 33:6092–6099Google Scholar
  19. Cade-Menun BJ, Paytan A (2010) Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Mar Chem 121:27–36Google Scholar
  20. Cakmak T, Angun P, Demiray YE, Ozkan AD, Elibol Z, Tekinay T (2012) Differential effects of nitrogen and sulfur deprivation on growth and biodiesel feedstock production of Chlamydomonas reinhardtii. Biotechnol Bioeng 109:1947–1957PubMedGoogle Scholar
  21. Caperon J, Meyer J (1972) Nitrogen-limited growth of marine phytoplankton—I. Changes in population characteristics with steady-state growth rate. Deep Sea Res Oceanogr Abstr 19:601–632Google Scholar
  22. Cárdenas J, Rivas J, Paneque A, Losada M (1972) Effect of iron supply on the activities of the nitrate-reducing system from Chlorella. Arch Microbiol 81:260–263Google Scholar
  23. Carfagna S, Salbitani G, Vona V, Esposito S (2011) Changes in cysteine and O-acetyl-l-serine levels in the microalga Chlorella sorokiniana in response to the S-nutritional status. J Plant Physiol 168:2188–2195PubMedGoogle Scholar
  24. Chen M, Tang H, Ma H, Holland TC, Ng KYS, Salley SO (2011) Effect of nutrients on growth and lipid accumulation in the green algae Dunaliella tertiolecta. Bioresour Technol 102:1649–1655PubMedGoogle Scholar
  25. Choi G-G, Kim B-H, Ahn C-Y, Oh H-M (2011) Effect of nitrogen limitation on oleic acid biosynthesis in Botryococcus braunii. J Appl Phycol 23:1031–1037Google Scholar
  26. Chojnacka K (2007) Using biosorption to enrich the biomass of Chlorella vulgaris with microelements to be used as mineral feed supplement. World J Microbiol Biotechnol 23:1139–1147Google Scholar
  27. Davies J, Grossman A (2004) Responses to deficiencies in macronutrients. In: Rochaix J, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas, vol 7. Advances in photosynthesis and respiration. Springer, Netherlands, pp 613–635Google Scholar
  28. Del Campo JA, Moreno J, Rodríguez H, Angeles Vargas M, Rivas J, Guerrero MG (2000) Carotenoid content of chlorophycean microalgae: factors determining lutein accumulation in Muriellopsis sp. (Chlorophyta). J Biotechnol 76:51–59PubMedGoogle Scholar
  29. Del Campo J, García-González M, Guerrero M (2007) Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 74:1163–1174PubMedGoogle Scholar
  30. DeMott W, Van Donk E (2013) Strong interactions between stoichiometric constraints and algal defenses: evidence from population dynamics of Daphnia and algae in phosphorus-limited microcosms. Oecologia 171:175–186Google Scholar
  31. Deng X, Fei X, Li Y (2011) The effects of nutritional restriction on neutral lipid accumulation in Chlamydomonas and Chlorella. Afr J Microbiol Res 5:260–270Google Scholar
  32. Di Martino Rigano V, Vona V, Carfagna S, Esposito S, Carillo P, Rigano C (2000) Effects of sulfate-starvation and re-supply on growth, NH4 + uptake and starch metabolism in Chlorella sorokiniana. Funct Plant Biol 27:335–342Google Scholar
  33. Doucha J, Lívanský K (2006) Productivity, CO2/O2 exchange and hydraulics in outdoor open high density microalgal (Chlorella sp.) photobioreactors operated in a Middle and Southern European climate. J Appl Phycol 18:811–826Google Scholar
  34. Doucha J, Lívanský K, Kotrbáček V, Zachleder V (2009) Production of Chlorella biomass enriched by selenium and its use in animal nutrition: a review. Appl Microbiol Biotechnol 83:1001–1008PubMedGoogle Scholar
  35. Doušková I, Hlavová M, Umysová D, Vítová M, Zachleder V (2009a) Industrial strain Scenedesmus quadricauda SeIV of green chlorococcal alga Scenedesmus quadricauda (Turp.) Bréb. Czech Republic Patent 300861, 13.05.2009Google Scholar
  36. Doušková I, Hlavová M, Umysová D, Vítová M, Zachleder V (2009b) Industrial strain Scenedesmus quadricauda SeIV+VI of green chlorococcal alga Scenedesmus quadricauda (Turp.) Bréb. Czech Republic Patent 300808, 13.05.2009Google Scholar
  37. Doušková I, Hlavová M, Umysová D, Vítová M, Zachleder V (2009c) Industrial strain Scenedesmus quadricauda SeVI of green chlorococcal alga Scenedesmus quadricauda (Turp.) Bréb. Czech Republic Patent 300809, 13.05.2009Google Scholar
  38. Dragone G, Fernandes BD, Abreu AP, Vicente AA, Teixeira JA (2011) Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Appl Energy 88:3331–3335Google Scholar
  39. Droop MR (1973) Some thoughts on nutrient limitation in algae. J Phycol 9:264–272Google Scholar
  40. Droop MR (1983) 25 years of algal growth kinetics: a personal view. Bot Mar 26:99–112Google Scholar
  41. Eixler S, Karsten U, Selig U (2006) Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cells and its dependence on phosphate supply. Phycologia 45:53–60Google Scholar
  42. Elsheek MM, Rady AA (1995) Effect of phosphorus starvation on growth, photosynthesis and some metabolic processes in the unicellular green-alga Chlorella kessleri. Phyton 35:139–151Google Scholar
  43. Estevez MS, Malanga G, Puntarulo S (2001) Iron-dependent oxidative stress in Chlorella vulgaris. Plant Sci 161:9–17Google Scholar
  44. Feng Y, Li C, Zhang D (2011) Lipid production of Chlorella vulgaris cultured in artificial wastewater medium. Bioresour Technol 102:101–105PubMedGoogle Scholar
  45. Fernandes B, Teixeira J, Dragone G, Vicente AA, Kawano S, Bišová K, Přibyl P, Zachleder V, Vítová M (2013) Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri. Bioresour Technol 144:268–274PubMedGoogle Scholar
  46. Fernandez E, Galvan A (2007) Inorganic nitrogen assimilation in Chlamydomonas. J Exp Bot 58:2279–2287PubMedGoogle Scholar
  47. Fernie AR, Obata T, Allen AE, Araújo WL, Bowler C (2012) Leveraging metabolomics for functional investigations in sequenced marine diatoms. Trends Plant Sci 17:395–403PubMedGoogle Scholar
  48. Flynn KJ (1990) The determination of nitrogen status in microalgae. Mar Ecol Prog Ser 61:297–307Google Scholar
  49. Fournier E, Adam-Guillermin C, Potin-Gautier M, Pannier F (2010) Selenate bioaccumulation and toxicity in Chlamydomonas reinhardtii: influence of ambient sulphate ion concentration. Aquat Toxicol 97:51–57PubMedGoogle Scholar
  50. Franco AR, Cárdenas J, Fernández E (1988) Two different carriers transport both ammonium and methylammonium in Chlamydomonas reinhardtii. J Biol Chem 263:14039–14043PubMedGoogle Scholar
  51. Galván A, Quesada A, Fernández E (1996) Nitrate and nitrite are transported by different specific transport systems and by a bispecific transporter in Chlamydomonas reinhardtii. J Biol Chem 271:2088–2092PubMedGoogle Scholar
  52. Geoffroy L, Gilbin R, Simon O, Floriani M, Adam C, Pradines C, Cournac L, Garnier-Laplace J (2007) Effect of selenate on growth and photosynthesis of Chlamydomonas reinhardtii. Aquat Toxicol 83:149–158PubMedGoogle Scholar
  53. Giordano M, Pezzoni V, Hell R (2000) Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol 124:857–864PubMedCentralPubMedGoogle Scholar
  54. Gómez-Jacinto V, Arias-Borrego A, García-Barrera T, Garbayo I, Vílchez C, Gómez-Ariza JL (2010) Iodine speciation in iodine-enriched microalgae Chlorella vulgaris. Pure Appl Chem 82:473–481Google Scholar
  55. González-Fernández C, Ballesteros M (2012) Linking microalgae and cyanobacteria culture conditions and key-enzymes for carbohydrate accumulation. Biotechnol Adv 30:1655–1661PubMedGoogle Scholar
  56. Griffiths M, Hille R, Harrison SL (2012) Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. J Appl Phycol 24:989–1001Google Scholar
  57. Grobbelaar JU (2004) Algal nutrition: mineral nutrition. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science, London, pp 97–115Google Scholar
  58. Han F, Huang J, Li Y, Wang W, Wan M, Shen G, Wang J (2013) Enhanced lipid productivity of Chlorella pyrenoidosa through the culture strategy of semi-continuous cultivation with nitrogen limitation and pH control by CO2. Bioresour Technol 136:418–424PubMedGoogle Scholar
  59. Harwood JL, Nicholls RG (1979) The plant sulpholipid: a major component of the sulphur cycle. Biochem Soc Trans 7:440–447PubMedGoogle Scholar
  60. Ho S-H, Chen W-M, Chang J-S (2010) Scenedesmus obliquus CNW-N as a potential candidate for CO2 mitigation and biodiesel production. Bioresour Technol 101:8725–8730PubMedGoogle Scholar
  61. Ho S-H, Huang S-W, Chen C-Y, Hasunuma T, Kondo A, Chang J-S (2013) Bioethanol production using carbohydrate-rich microalgae biomass as feedstock. Bioresour Technol 135:191–198PubMedGoogle Scholar
  62. Hockin NL, Mock T, Mulholland F, Kopriva S, Malin G (2012) The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants. Plant Physiol 158:299–312PubMedCentralPubMedGoogle Scholar
  63. Hu Q (2004) Environmental effects on cell composition. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science, London, pp 83–94Google Scholar
  64. Hu Q, Sommerfeld M, Jarvis E, Ghirardi M, Posewitz M, Seibert M, Darzins A (2008) Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J 54:621–639PubMedGoogle Scholar
  65. Iriani D, Suriyaphan O, Chaiyanate N (2011) Effect of iron concentration on growth, protein content and total phenolic content of Chlorella sp. cultured in basal medium. Sains Malays 40:353–358Google Scholar
  66. Jian-Ming L, Cheng L-H, Xu X-H, Zhang L, Chen H-L (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101:6797–6804Google Scholar
  67. Kauss H (1987) Some aspects of calcium-dependent regulation in plant metabolism. Annu Rev Plant Physiol 38:47–71Google Scholar
  68. Khozin-Goldberg I, Iskandarov U, Cohen Z (2011) LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology. Appl Microbiol Biotechnol 91:905–915PubMedGoogle Scholar
  69. Kirk DL, Kirk MM (1978) Carrier-mediated uptake of arginine and urea by Chlamydomonas reinhardtii. Plant Physiol 61:556–560PubMedCentralPubMedGoogle Scholar
  70. Koller M, Salerno A, Tuffner P, Koinigg M, Böchzelt H, Schober S, Pieber S, Schnitzer H, Mittelbach M, Braunegg G (2012) Characteristics and potential of microalgal cultivation strategies: a review. J Clean Prod 37:377–388Google Scholar
  71. Kotrbáček V, Doucha J, Offenbartil T (2004) Use of Chlorella as a carrier of organic-bound iodine in the nutrition of sows. Czech J Anim Sci 49:28–32Google Scholar
  72. Krauss F, Schmidt A (1987) Sulphur sources for growth of Chlorella fusca and their influence on key enzymes of sulphur metabolism. J Gen Microbiol 133:1209–1219Google Scholar
  73. Kruskopf MM, Du Plessis S (2004) Induction of both acid and alkaline phosphatase activity in two green-algae (Chlorophyceae) in low N and P concentrations. Hydrobiologia 513:59–70Google Scholar
  74. La Fontaine S, Quinn JM, Nakamoto SS, Page MD, Göhre V, Moseley JL, Kropat J, Merchant S (2002) Copper-dependent iron assimilation pathway in the model photosynthetic eukaryote Chlamydomonas reinhardtii. Eukaryot Cell 1:736–757PubMedCentralPubMedGoogle Scholar
  75. Lamers PP, Janssen M, De Vos RCH, Bino RJ, Wijffels RH (2008) Exploring and exploiting carotenoid accumulation in Dunaliella salina for cell-factory applications. Trends Biotechnol 26:631–638PubMedGoogle Scholar
  76. Lamers PP, van de Laak CCW, Kaasenbrood PS, Lorier J, Janssen M, De Vos RCH, Bino RJ, Wijffels RH (2010) Carotenoid and fatty acid metabolism in light-stressed Dunaliella salina. Biotechnol Bioeng 106:638–648PubMedGoogle Scholar
  77. Lamers PP, Janssen M, De Vos RCH, Bino RJ, Wijffels RH (2012) Carotenoid and fatty acid metabolism in nitrogen-starved Dunaliella salina, a unicellular green microalga. J Biotechnol 162:21–27PubMedGoogle Scholar
  78. Laws E, Bannister T (1980) Nutrient- and light-limited growth of Thalassiosira fluviatilis in continuous culture, with implications for phytoplankton growth in the ocean. Limnol Oceanogr 25:457–473Google Scholar
  79. Lee T-M, Liu C-H (1999) Correlation of decreased calcium contents with proline accumulation in the marine green macroalga Ulva fasciata exposed to elevated NaCl contents in seawater. J Exp Bot 50:1855–1862Google Scholar
  80. Leustek T, Martin MN, Bick J-A, Davies JP (2000) Pathways and regulation of sulfur metabolism revealed through molecular genetic studies. Annu Rev Plant Physiol 51:141–165Google Scholar
  81. Li Y, Horsman M, Wang B, Wu N, Lan C (2008) Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Appl Microbiol Biotechnol 81:629–636PubMedGoogle Scholar
  82. Li Y, Han D, Sommerfeld M, Hu Q (2011) Photosynthetic carbon partitioning and lipid production in the oleaginous microalga Pseudochlorococcum sp. (Chlorophyceae) under nitrogen-limited conditions. Bioresour Technol 102:123–129PubMedGoogle Scholar
  83. Li X, Přibyl P, Bišová K, Kawano S, Cepák V, Zachleder V, Čížková M, Brányiková I, Vítová M (2012) The microalga Parachlorella kessleri—a novel highly efficient lipid producer. Biotechnol Bioeng 110:97–107PubMedGoogle Scholar
  84. Liang K, Zhang Q, Gu M, Cong W (2013) Effect of phosphorus on lipid accumulation in freshwater microalga Chlorella sp. J Appl Phycol 25:311–318Google Scholar
  85. Lin Q, Lin J (2011) Effects of nitrogen source and concentration on biomass and oil production of a Scenedesmus rubescens like microalga. Bioresour Technol 102:1615–1621PubMedGoogle Scholar
  86. Lin Q, Gu N, Lin J (2012) Effect of ferric ion on nitrogen consumption, biomass and oil accumulation of a Scenedesmus rubescens-like microalga. Bioresour Technol 112:242–247PubMedGoogle Scholar
  87. Liu Z-Y, Wang G-C, Zhou B-C (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722PubMedGoogle Scholar
  88. Low SC, Berry MJ (1996) Knowing when not to stop: selenocysteine incorporation in eukaryotes. Trends Biochem Sci 21:203–208PubMedGoogle Scholar
  89. Maillard P, Thepenier C, Gudin C (1993) Determination of an ethylene biosynthesis pathway in the unicellular green alga, Haematococcus pluvialis. Relationship between growth and ethylene production. J Appl Phycol 5:93–98Google Scholar
  90. Mandal S, Mallick N (2009) Microalga Scenedesmus obliquus as a potential source for biodiesel production. Appl Microbiol Biotechnol 84:281–291PubMedGoogle Scholar
  91. Markou G, Chatzipavlidis I, Georgakakis D (2012) Carbohydrates production and bio-flocculation characteristics in cultures of Arthrospira (Spirulina) platensis: improvements through phosphorus limitation process. Bioenerg Res 1–11Google Scholar
  92. Maršálková B, Širmerová M, Kuřec M, Brányik T, Brányiková I, Melzoch K, Zachleder V (2010) Microalgae Chlorella sp. as an alternative source of fermentable sugars. Chem Eng Trans 21:1279–1284Google Scholar
  93. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232Google Scholar
  94. Metzger P, Largeau C (2005) Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl Microbiol Biotechnol 66:486–496PubMedGoogle Scholar
  95. Miao X, Wu Q (2004) High yield bio-oil production from fast pyrolysis by metabolic controlling of Chlorella protothecoides. J Biotechnol 110:85–93PubMedGoogle Scholar
  96. Milinki E, Molnár S, Kiss A, Virág D, Pénez-Kónya E (2011) Study of microelement accumulating characteristics of microalgae. Acta Bot Hung 53:159–167Google Scholar
  97. Morlon H, Fortin C, Floriani M, Adam C, Garnier-Laplace J, Boudou A (2005) Toxicity of selenite in the unicellular green alga Chlamydomonas reinhardtii: comparison between effects at the population and sub-cellular level. Aquat Toxicol 73:65–78PubMedGoogle Scholar
  98. Morris I (1974) Nitrogen assimilation and protein synthesis. In: Stewart WDP (ed) Algal physiology and biochemistry. University of California Press, Berkeley, pp 560–582Google Scholar
  99. Morrissey J, Bowler C (2012) Iron utilization in marine cyanobacteria and eukaryotic algae. Front Microbiol 3:43. doi: 10.3389/fmicb.2012.00043 PubMedCentralPubMedGoogle Scholar
  100. Moseley J, Grossman AR (2009) Phosphate metabolism and responses to phosphorus deficiency. In: The Chlamydomonas sourcebook: organellar and metabolic processes, vol 2, 2nd edn. Academic Press, New York, pp 189–215Google Scholar
  101. Mujtaba G, Choi W, Lee C-G, Lee K (2012) Lipid production by Chlorella vulgaris after a shift from nutrient-rich to nitrogen starvation conditions. Bioresour Technol 123:279–283PubMedGoogle Scholar
  102. Muñoz-Blanco J, Hidalgo-Martínez J, Cárdenas J (1990) Extracellular deamination of l-amino acids by Chlamydomonas reinhardtii cells. Planta 182:194–198PubMedGoogle Scholar
  103. Neumann PM, De Souza MP, Pickering IJ, Terry N (2003) Rapid microalgal metabolism of selenate to volatile dimethylselenide. Plant Cell Environ 26:897–905PubMedGoogle Scholar
  104. Niedobová E, Machát J, Kanický V, Otruba V (2005) Determination of iodine in enriched Chlorella by ICP-OES in the VUV region. Microchim Acta 150:103–107Google Scholar
  105. Palmqvist K, Yu J-W, Badger MR (1994) Carbonic anhydrase activity and inorganic carbon fluxes in low- and high-C1 cells of Chlamydomonas reinhardtii and Scenedesmus obliquus. Physiol Plant 90:537–547Google Scholar
  106. Pawlik-Skowrońska B (2003) When adapted to high zinc concentrations the periphytic green alga Stigeoclonium tenue produces high amounts of novel phytochelatin-related peptides. Aquat Toxicol 62:155–163PubMedGoogle Scholar
  107. Pinto E, Sigaud-kutner TCS, Leitão MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018Google Scholar
  108. Plumley FG, Schmidt GW (1989) Nitrogen-dependent regulation of photosynthetic gene expression. Proc Natl Acad Sci U S A 86:2678–2682PubMedCentralPubMedGoogle Scholar
  109. Powell N, Shilton AN, Pratt S, Chisti Y (2008) Factors influencing luxury uptake of phosphorus by microalgae in waste stabilization ponds. Environ Sci Technol 42:5958–5962PubMedGoogle Scholar
  110. Powell N, Shilton A, Chisti Y, Pratt S (2009) Towards a luxury uptake process via microalgae–defining the polyphosphate dynamics. Water Res 43:4207–4213PubMedGoogle Scholar
  111. Přibyl P, Cepák V, Zachleder V (2012) Production of lipids in 10 strains of Chlorella and Parachlorella and enhanced lipid productivity in Chlorella vulgaris. Appl Microbiol Biotechnol 94:549–561PubMedGoogle Scholar
  112. Ratha SK, Prasanna R, Prasad RBN, Sarika C, Dhar DW, Saxena AK (2013) Modulating lipid accumulation and composition in microalgae by biphasic nitrogen supplementation. Aquaculture 392–395:69–76Google Scholar
  113. Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynth Res 60:111–149Google Scholar
  114. Reunova Y, Aizdaicher N, Khristoforova N, Reunov A (2007) Effects of selenium on growth and ultrastructure of the marine unicellular alga Dunaliella salina (Chlorophyta). Russ J Mar Biol 33:125–132Google Scholar
  115. Richards RG, Mullins BJ (2013) Using microalgae for combined lipid production and heavy metal removal from leachate. Ecol Model 249:59–67Google Scholar
  116. Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112PubMedGoogle Scholar
  117. Rosenberg JN, Oyler GA, Wilkinson L, Betenbaugh MJ (2008) A green light for engineered algae: redirecting metabolism to fuel a biotechnology revolution. Curr Opin Biotechnol 19:430–436PubMedGoogle Scholar
  118. Ruangsomboon S, Ganmanee M, Choochote S (2013) Effects of different nitrogen, phosphorus, and iron concentrations and salinity on lipid production in newly isolated strain of the tropical green microalga, Scenedesmus dimorphus KMITL. J Appl Phycol 25:867–874Google Scholar
  119. Schrauzer GN (2001) Nutritional selenium supplements: product types, quality, and safety. J Am Coll Nutr 20:1–4PubMedGoogle Scholar
  120. Šetlík I, Ballin G, Doucha J, Zachleder V (1988) Macromolecular syntheses and the course of cell cycle events in the chlorococcal alga Scenedesmus quadricauda under nutrient starvation: effect of sulphur starvation. Biol Plant 30:161–169Google Scholar
  121. Seufferheld MJ, Alvarez HM, Farias ME (2008) Role of polyphosphates in microbial adaptation to extreme environments. Appl Environ Microbiol 74:5867–5874PubMedCentralPubMedGoogle Scholar
  122. Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553Google Scholar
  123. Siderius M, Musgrave A, van den Ende H, Koerten H, Cambier P, van der Meer P (1996) Chlamydomonas eugametos (Chlorophyta) stores phopshate in polphosphate bodies together with calcium1. J Phycol 32:402–409Google Scholar
  124. Sigee DC, Bahrami F, Estrada B, Webster RE, Dean AP (2007) The influence of phosphorus availability on carbon allocation and P quota in Scenedesmus subspicatus: a synchrotron-based FTIR analysis. Phycologia 46:583–592Google Scholar
  125. Sirisansaneeyakul S, Singhasuwan S, Choorit W, Phoopat N, Garcia J, Chisti Y (2011) Photoautotrophic production of lipids by some Chlorella strains. Mar Biotechnol 13:928–941PubMedGoogle Scholar
  126. Siron R, Giusti G, Berland B (1989) Changes in the fatty acid composition of Phaeodactylum tricornutum and Dunaliella tertiolecta during growth and under phosphorus deficiency. Mar Ecol Prog Ser 55:95–100Google Scholar
  127. Soeder CJ, Hegewald E, Kneifel H (1987) Green microalgae can use naphthalenesulfonic acids as sources of sulfur. Arch Microbiol 148:260–263Google Scholar
  128. Solovchenko AE, Khozin-Goldberg I, Didi-Cohen S, Cohen Z, Merzlyak MN (2008) Effects of light intensity and nitrogen starvation on growth, total fatty acids and arachidonic acid in the green microalga Parietochloris incisa. J Appl Phycol 20:245–251Google Scholar
  129. Stefels J, van Leeuwe MA (1998) Effects of iron and light stress on the biochemical composition of antarctic Phaeocystis sp. (Prymnesiophyceae): I. Intracellular DSMP concentrations. J Phycol 34:486–495Google Scholar
  130. Sterner RW, Smutka TM, McKay RML, Xiaoming Q, Brown ET, Sherrell RM (2004) Phosphorus and trace metal limitation of algae and bacteria in Lake Superior. Limnol Oceanogr 49:495–507Google Scholar
  131. Sunda WG, Huntsman SA (2004) Relationships among photoperiod, carbon fixation, growth, chlorophyll a, and cellular iron and zinc in a coastal diatom. Limnol Oceanogr 49:1742–1753Google Scholar
  132. Sunda WG, Neil MP, Francois MMM (2005) Trace metal ion buffers and their use in culture. In: Anderson RA (ed) Algal culturing techniques. Elsevier Academic Press, San Diego, pp 35–64Google Scholar
  133. Tababa HG, Hirabayashi S, Inobushi K (2012) Media optimization of Parietochloris incisa for arachidonic acid accumulation in an outdoor vertical tubular photobioreactor. J Appl Phycol 24:887–895PubMedCentralPubMedGoogle Scholar
  134. Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184PubMedGoogle Scholar
  135. Tan Y, Lin J (2011) Biomass production and fatty acid profile of a Scenedesmus rubescens-like microalga. Bioresour Technol 102:10131–10135PubMedGoogle Scholar
  136. Tang H, Chen M, Garcia MED, Abunasser N, Ng KYS, Salley SO (2011) Culture of microalgae Chlorella minutissima for biodiesel feedstock production. Biotechnol Bioeng 108:2280–2287Google Scholar
  137. Theodorou ME, Elrifi IR, Turpin DH, Plaxton WC (1991) Effects of phosphorus limitation on respiratory metabolism in the green alga Selenastrum minutum. Plant Physiol 95:1089–1095PubMedCentralPubMedGoogle Scholar
  138. Tran H-L, Kwon J-S, Kim ZH, Oh Y, Lee C-G (2010) Statistical optimization of culture media for growth and lipid production of Botryococcus braunii LB572. Biotechnol Bioproc Eng 15:277–284Google Scholar
  139. Tredici MR (2004) Mass production of microalgae: photobioreactors. In: Richmond A (ed) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Science, London, pp 178–214Google Scholar
  140. Twiss MR, Nalewajko C (1992) Influence of phosphorus nutrition on copper toxicity to three strains of Scenedesmus acutus (Chlorophyceae). J Phycol 28:291–298Google Scholar
  141. Umysová D, Vítová M, Doušková I, Bišová K, Hlavová M, Čížková M, Machát J, Doucha J, Zachleder V (2009) Bioaccumulation and toxicity of selenium compounds in the green alga Scenedesmus quadricauda. BMC Plant Biol 9:58PubMedCentralPubMedGoogle Scholar
  142. Wang W-X, Dei RCH (2006) Metal stoichiometry in predicting Cd and Cu toxicity to a freshwater green alga Chlamydomonas reinhardtii. Environ Pollut 142:303–312PubMedGoogle Scholar
  143. Wang ZT, Ullrich N, Joo S, Waffenschmidt S, Goodenough U (2009) Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starch-less Chlamydomonas reinhardtii. Eukaryot Cell 8:1856–1868PubMedCentralPubMedGoogle Scholar
  144. Webster RE, Dean AP, Pittman JK (2011) Cadmium exposure and phosphorus limitation increases metal content in the freshwater alga Chlamydomonas reinhardtii. Environ Sci Technol 45:7489–7496PubMedGoogle Scholar
  145. Wheeler AE, Zingaro RA, Irgolic K, Bottino NR (1982) The effect of selenate, selenite, and sulfate on the growth of 6 unicellular marine-species. J Exp Mar Biol Ecol 57:181–194Google Scholar
  146. Wong D, Olivesra L (1991) Effects of selenite and selenate on the growth and motility of seven species of marine microalgae. Can J Fish Aquat Sci 48:1193–1200Google Scholar
  147. Worms I, Simon DF, Hassler CS, Wilkinson KJ (2006) Bioavailability of trace metals to aquatic microorganisms: importance of chemical, biological and physical processes on biouptake. Biochimie 88:1721–1731PubMedGoogle Scholar
  148. Wu Y-H, Yu Y, Li X, Hu H-Y, Su Z-F (2012) Biomass production of a Scenedesmus sp. under phosphorous-starvation cultivation condition. Bioresour Technol 112:193–198Google Scholar
  149. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139PubMedCentralPubMedGoogle Scholar
  150. Xin L, Hong-ying H, Ke G, Ying-xue S (2010) Effects of different nitrogen and phosphorus concentrations on the growth, nutrient uptake, and lipid accumulation of a freshwater microalga Scenedesmus sp. Bioresour Technol 101:5494–5500PubMedGoogle Scholar
  151. Yadavalli V, Jolley CC, Malleda C, Thangaraj B, Fromme P, Subramanyam R (2012) Alteration of proteins and pigments influence the function of photosystem I under iron deficiency from Chlamydomonas reinhardtii. PLoS ONE. doi: 10.1371/journal.pone.0035084 Google Scholar
  152. Yamaoka Y, Takimura O, Fuse H, Kamimura K (1990) Accumulation of arsenic and selenium by Dunaliella sp. Appl Organomet Chem 4:261–264Google Scholar
  153. Yang S, Wang J, Cong W, Cai Z, Ouyang F (2004a) Effects of bisulfite and sulfite on the microalga Botryococcus braunii. Enzym Microb Technol 35:46–50Google Scholar
  154. Yang S, Wang J, Cong W, Cai Z, Ouyang F (2004b) Utilization of nitrite as a nitrogen source by Botryococcus braunii. Biotechnol Lett 26:239–243PubMedGoogle Scholar
  155. Yao C, Ai J, Cao X, Xue S, Zhang W (2012) Enhancing starch production of a marine green microalga Tetraselmis subcordiformis through nutrient limitation. Bioresour Technol 118:438–444PubMedGoogle Scholar
  156. Yao C-H, Ai J-N, Cao X-P, Xue S (2013) Characterization of cell growth and starch production in the marine green microalga Tetraselmis subcordiformis under extracellular phosphorus-deprived and sequentially phosphorus-replete conditions. Appl Microbiol Biotechnol 97:6099–6110PubMedGoogle Scholar
  157. Yeesang C, Cheirsilp B (2011) Effect of nitrogen, salt, and iron content in the growth medium and light intensity on lipid production by microalgae isolated from freshwater sources in Thailand. Bioresour Technol 102:3034–3040PubMedGoogle Scholar
  158. Yildiz FH, Davies JP, Grossman AR (1994) Characterization of sulfate transport in Chlamydomonas reinhardtii during sulfur-limited and sulfur-sufficient growth. Plant Physiol 104:981–987PubMedCentralPubMedGoogle Scholar
  159. Zachleder V, Ballin G, Doucha J, Šetlík I (1988) Macromolecular syntheses and the course of cell cycle events in the chlorococcal alga Scenedesmus quadricauda under nutrient starvation: effect of phosphorus starvation. Biol Plant 30:92–99Google Scholar
  160. Zhang Z, Shrager J, Jain M, Chang C-W, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348PubMedCentralPubMedGoogle Scholar
  161. Zhou X, Ge H, Xia L, Zhang D, Hu C (2013) Evaluation of oil-producing algae as potential biodiesel feedstock. Bioresour Technol 134:24–29PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Gita Procházková
    • 1
  • Irena Brányiková
    • 1
  • Vilém Zachleder
    • 2
  • Tomáš Brányik
    • 1
    Email author
  1. 1.Department of BiotechnologyInstitute of Chemical Technology PraguePragueCzech Republic
  2. 2.Laboratory of Cell Cycles of Algae, Institute of MicrobiologyAcademy of Sciences of the Czech RepublicTřebonCzech Republic

Personalised recommendations