Characterization of cell growth and starch production in the marine green microalga Tetraselmis subcordiformis under extracellular phosphorus-deprived and sequentially phosphorus-replete conditions

Applied Microbiology and Biotechnology

Volumn 97, Issue 13, 2013, Pages 6099-6110

  Yao, Chang Hong ^a,b   Ai, Jiang Ning ^a   Cao, Xu Peng ^a   Xue, Song ^a  

^a DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

Initial cell density; Phosphorus; Productivity; Recovery; Starch; Tetraselmis subcordiformis

Indexed keywords

BIOMASS PRODUCTIVITY; CELL DENSITY; INTRACELLULAR PHOSPHORUS; PHOSPHORUS DEPRIVATIONS; PHOTOSYNTHETIC ACTIVITY; STARCH ACCUMULATION; STARCH CONCENTRATION; TETRASELMIS SUBCORDIFORMIS;

ALGAE; BIOMASS; CELL GROWTH; CELLS; CYTOLOGY; ENZYME ACTIVITY; GROWTH KINETICS; MOLECULAR BIOLOGY; PHOSPHORUS; PRODUCTIVITY; RECOVERY;

STARCH;

CHLOROPHYLL; NITRATE; NITROGEN; PHOSPHATE; PHOSPHORUS; POTASSIUM DIHYDROGEN PHOSPHATE; STARCH; SULFUR;

BIOFUEL; BIOLOGICAL PRODUCTION; BIOTECHNOLOGY; CYTOLOGY; GREEN ALGA; GROWTH; MARINE ENVIRONMENT; MICROALGA; PHOSPHORUS; STARCH;

ALGAL GROWTH; ARTICLE; BIOCHEMICAL COMPOSITION; BIOMASS PRODUCTION; CELL DENSITY; CELL GROWTH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENVIRONMENTAL FACTOR; GREEN ALGA; MICROALGA; MICROBIAL METABOLISM; NONHUMAN; NUTRIENT AVAILABILITY; PHOTOSYNTHESIS; TETRASELMIS SUBCORDIFORMIS;

BIOMASS; CHLOROPHYTA; CULTURE MEDIA; PHOSPHORUS; STARCH; STRESS, PHYSIOLOGICAL;

TETRASELMIS SUBCORDIFORMIS;

EID: 84879416233     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-013-4983-x     Document Type: Article

References (47)

1. Aikawa S, Izumi Y, Matsuda F, Hasunuma T, Chang JS, Kondo A (2012) Synergistic enhancement of glycogen production in Arthrospira platensis by optimization of light intensity and nitrate supply. Bioresour Technol 108:211-215. doi: 10.1016/j.biortech.2012.01.004
2. Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89-113. doi: 10.1146/annurev.arplant.59.032607. 092759
3. Ball SG (1998) Regulation of starch biosynthesis. In: Rochaix JD, Goldschmidt-Clermont M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydomonas. Kluwer, The Netherlands, pp 549-567
4. Ball SG, Dirick L, Decq A, Martiat J-C, Matagne R (1990) Physiology of starch storage in the monocellular alga Chlamydomonas reinhardtii. Plant Sci 66:1-9. doi: 10.1016/0168-9452(90)90162-H
5. Ball SG, Morell MK (2003) From bacterial glycogen to starch: understanding the biogenesis of the plant starch granule. Annu Rev Plant Biol 54:207-233. doi: 10.1146/annurev.arplant.54.031902.134927
6. Brányiková I, Maršálková B, Doucha J, Brányik T, Bišová K, Zachleder V, Vítová M (2011) Microalgae - novel highly efficient starch producers. Biotechnol Bioeng 108:766-776. doi: 10.1002/bit.23016
7. Chen Y, Wang J, Liu T, Gao L (2012) Effects of initial population density (IPD) on growth and lipid composition of Nannochloropsis sp. J Appl Phycol 24:1623-1627. doi: 10.1007/s10811-012-9825-1
8. Couso I, Vila M, Vigara J, Cordero BF, Vargas MÁ, Rodríguez H, León R (2012) Synthesis of carotenoids and regulation of the carotenoid biosynthesis pathway in response to high light stress in the unicellular microalga Chlamydomonas reinhardtii. Eur J Phycol 47:223-232. doi: 10.1080/09670262.2012.692816
9. Dean AP, Estrada B, Nicholson JM, Sigee DC (2008a) Molecular response of Anabaena flos-aquae to differing concentrations of phosphorus: a combined Fourier transform infrared and X-ray microanalytical study. Phycol Res 56:193-201. doi: 10.1111/j.1440-1835.2008.00501.x
10. Dean AP, Nicholson JM, Sigee DC (2008b) Impact of phosphorus quota and growth phase on carbon allocation in Chlamydomonas reinhardtii: an FTIR microspectroscopy study. Eur J Phycol 43:345-354. doi: 10.1080/09670260801979287
11. Doan QC, Moheimani NR, Mastrangelo AJ, Lewis DM (2012) Microalgal biomass for bioethanol fermentation: implications for hypersaline systems with an industrial focus. Biomass Bioenergy 46:79-88. doi: 10.1016/j.biombioe.2012.08. 022
12. Dragone G, Fernandes BD, Abreu AP, Vicente AA, Teixeira JA (2011) Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Appl Energy 88:3331-3335. doi: 10.1016/j.apenergy.2011.03.012
13. Eixler S, Karsten U, Selig U (2006) Phosphorus storage in Chlorella vulgaris (Trebouxiophyceae, Chlorophyta) cells and its dependence on phosphate supply. Phycologia 45:53-60. doi: 10.2216/04-79.1
14. Fan J, Yan C, Andre C, Shanklin J, Schwender J, Xu C (2012) Oil accumulation is controlled by carbon precursor supply for fatty acid synthesis in Chlamydomonas reinhardtii. Plant Cell Physiol 53:1380-1390. doi: 10.1093/pcp/pcs082
15. Furbank RT, Lilley RM (1980) Effects of inorganic phosphate on the photosynthetic carbon reduction cycle in extracts from the stroma of pea chloroplasts. Biochim Biophys Acta 592:65-75. doi: 10.1016/0005-2728(80)90114-0
16. Ho SH, Huang SW, Chen CY, Hasunuma T, Kondo A, Chang JS (2012) Characterization and optimization of carbohydrate production from an indigenous microalga Chlorella vulgaris FSP-E. Bioresour Technol. doi: 10.1016/j.biortech. 2012.10.100
17. Hu Q, Richmond A (1994) Optimizing the population density in Isochrysis galbana grown outdoors in a glass column photobioreactor. J Appl Phycol 6:391-396. doi: 10.1007/bf02182155
18. Hu Q, Richmond A (1996) Productivity and photosynthetic efficiency of Spirulina platensis as affected by light intensity, algal density and rate of mixing in a flat plate photobioreactor. J Appl Phycol 8:139-145. doi: 10.1007/bf02186317
19. John RP, Anisha GS, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102:186-193. doi: 10.1016/j.biortech.2010.06.139
20. Li X, Přibyl P, Bišová K, Kawano S, Cepák V, Zachleder V, Čížková M, Brányiková I, Vítová M (2013) The microalga Parachlorella kessleri - a novel highly efficient lipid producer. Biotechnol Bioeng 110:97-107. doi: 10.1002/bit.24595
21. 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 102:123-129. doi: 10.1016/j.biortech.2010.06.036
22. Li Y, Horsman M, Wang B, Wu N, Lan CQ (2008) Effects of nitrogen sources on cell growth and lipid accumulation of green alga Neochloris oleoabundans. Appl Microbiol Biotechnol 81:629-636. doi: 10.1007/s00253-008-1681-1
23. Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591-592. doi: 10.1042/bst0110591
24. Markou G (2012) Alteration of the biomass composition of Arthrospira (Spirulina) platensis under various amounts of limited phosphorus. Bioresour Technol 116:533-535. doi: 10.1016/j.biortech.2012.04.022
25. Markou G, Angelidaki I, Georgakakis D (2012a) Microalgal carbohydrates: an overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Appl Microbiol Biotechnol 96:631-645. doi: 10.1007/s00253-012-4398-0
26. Markou G, Chatzipavlidis I, Georgakakis D (2012b) Carbohydrates production and bio-flocculation characteristics in cultures of Arthrospira (Spirulina) platensis: improvements through phosphorus limitation process. Bioenergy Res 5:915-925. doi: 10.1007/s12155-012-9205-3
27. Markou G, Chatzipavlidis I, Georgakakis D (2012c) Effects of phosphorus concentration and light intensity on the biomass composition of Arthrospira (Spirulina) platensis. World J Microbiol Biotechnol 28:2661-2670. doi: 10.1007/s11274-012-1076-4
28. Moseley J, Grossman AR (2009) Phosphate metabolism and responses to phosphorus deficiency. In: Stern D (ed) The Chlamydomonas sourcebook: organellar and metabolic processes. vol 2, 2nd edn. Academic Press, New York, pp 189-215
29. Mussatto SI, Dragone G, Guimaraes PM, Silva JP, Carneiro LM, Roberto IC, Vicente A, Domingues L, Teixeira JA (2010) Technological trends, global market, and challenges of bio-ethanol production. Biotechnol Adv 28:817-830. doi: 10.1016/j.biotechadv.2010.07.001
30. Nielsen ES, Rochon T (1976) The Influence of extremely high concentrations of inorganic P at varying pH on the growth and photosynthesis of unicellular algae. Int Revue ges Hydrobiol 61:407-415. doi: 10.1002/iroh. 3510610402
31. Nigam PS, Singh A (2011) Production of liquid biofuels from renewable resources. Prog Energy Combust Sci 37:52-68. doi: 10.1016/j.pecs.2010.01.003
32. Nishikawa K, Machida H, Yamakoshi Y, Ohtomo R, Saito K, Saito M, Tominaga N (2006) Polyphosphate metabolism in an acidophilic alga Chlamydomonas acidophila KT-1 (Chlorophyta) under phosphate stress. Plant Sci 170:307-313. doi: 10.1016/j.plantsci.2005.08.025
33. Pal D, Khozin-Goldberg I, Cohen Z, Boussiba S (2011) The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl Microbiol Biotechnol 90:1429-1441. doi: 10.1007/s00253-011-3170-1
34. Pan YY, Wang ST, Chuang LT, Chang YW, Chen CN (2011) Isolation of thermo-tolerant and high lipid content green microalgae: oil accumulation is predominantly controlled by photosystem efficiency during stress treatments in Desmodesmus. Bioresour Technol 102:10510-10517. doi: 10.1016/j.biortech.2011.08. 091
35. Powell N, Shilton A, Chisti Y, Pratt S (2009) Towards a luxury uptake process via microalgae - defining the polyphosphate dynamics. Water Res 43:4207-4213. doi: 10.1016/j.watres.2009.06.011
36. Richmond A (2004) Biological principles of mass cultivation. In: Richmond A (ed) Handbook of microalgal mass culture: biotechnology and applied phycology. Blackwell, Oxford, pp 125-177
37. 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 102:100-112. doi: 10.1002/bit.22033
38. Rychter AM, Rao I (2005) Role of phosphorus in photosynthetic carbon metabolism. In: Pessarakli M (ed) Handbook of photosynthesis, 2nd edn. CRC Press, Florida, pp 123-148
39. Schreiber U (2004) Pulse-Amplitude-Modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: A signature of photosynthesis. Springer, The Netherland, pp 279-319
40. Shelly K, Holland D, Beardall J (2011) Assessing nutrient status of microalgae using chlorophyll a fluorescence. In: Suggett DJ, Prášil O, Borowitzka MA (eds) Chlorophyll a fluorescence in aquatic sciences: Methods and applications, vol 4. Springer, The Netherlands, pp 223-235
41. 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 46:583-592. doi: 10.2216/07-14.1
42. Solovchenko A, Khozin-Goldberg I, Recht L, Boussiba S (2011) Stress-induced changes in optical properties, pigment and fatty acid content of Nannochloropsis sp.: implications for non-destructive assay of total fatty acids. Mar Biotechnol 13:527-535. doi: 10.1007/s10126-010-9323-x
43. 2 bio-mitigation using microalgae. Appl Microbiol Biotechnol 79:707-718. doi: 10.1007/s00253-008-1518-y
44. Wang C, Kong H-N, He S-B, Zheng X-Y, Li C-J (2010) The inverse correlation between growth rate and cell carbohydrate content of Microcystis aeruginosa. J Appl Phycol 22:105-107. doi: 10.1007/s10811-009-9421-1
45. 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 112:193-198. doi: 10.1016/j.biortech.2012.02.037
46. Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129-139. doi: 10.1104/pp. 117.1.129
47. Yao CH, Ai JN, Cao XP, Xue S, Zhang W (2012) Enhancing starch production of a marine green microalga Tetraselmis subcordiformis through nutrient limitation. Bioresour Technol 118:438-444. doi: 10.1016/j.biortech.2012.05.030