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Effects of fundamental nutrient stresses on the lipid accumulation profiles in two diatom species Thalassiosira weissflogii and Chaetoceros muelleri

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Abstract

Microalgae are considered as attractive feedstocks for biofuel production nowadays because of their high lipid contents and easy cultivation. In the present study, two diatoms, Thalassiosira weissflogii and Chaetoceros muelleri, were cultured under various nutrient-limitation conditions to explore their comprehensive lipid accumulation profiles for further commercialization. In T. weissflogii, the highest neutral lipid accumulation and highest lipid productivity (14.28 mg L−1 day−1) were both recorded under P-limitation. In C. muelleri, the highest lipid content (35.03% of dry cell weight), highest neutral lipid accumulation, and highest lipid productivity (29.07 mg L−1 day−1) were all recorded under N-limitation. Besides, the predominant fatty acids of T. weissflogii and C. muelleri were myristic acid (C14:0), palmitic acid (C16:0), and palmitoleic acid (C16:1), with the amounts of 58.4–74.4 and 74.1–87.7% of the total fatty acids, respectively. Moreover, nutrient limitations led to a lower proportion of polyunsaturated fatty acids (PUFA) than that of saturated fatty acid (SFA) and monounsaturated fatty acid (MUFA) in both species. The ratios of (SFA + MUFA) to PUFA were from 1.65 to 3.01 in T. weissflogii, and up to 3.61 to 8.59 in C. muelleri. Our results suggested the feasibility of C. muelleri as biodiesel feedstock due to its more suitable fatty acid composition and higher lipid productivity compared to T. weissflogii.

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References

  1. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25(3):294–306

    Article  CAS  PubMed  Google Scholar 

  2. 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(4):621–639

    Article  CAS  PubMed  Google Scholar 

  3. Wang J, Seibert M (2017) Prospects for commercial production of diatoms. Biotechnol Biofuels 10(1):16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101(2):87–96

    Article  CAS  PubMed  Google Scholar 

  5. Rodolfi L, Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G, Tredici M (2009) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102(1):100–112

    Article  CAS  PubMed  Google Scholar 

  6. Guschina I, Harwood J (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45(2):160–186

    Article  CAS  PubMed  Google Scholar 

  7. Liang K, Zhang Q, Gu M, Cong W (2013) Effect of phosphorus on lipid accumulation in freshwater microalga Chlorella sp. J Appl Phycol 25(1):311–318

    Article  CAS  Google Scholar 

  8. Converti A, Casazza A, Ortiz E, Perego P, Del Borghi M (2009) Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem Eng Process 48(6):1146–1151

    Article  CAS  Google Scholar 

  9. Merzlyak M, Chivkunova O, Gorelova O, Reshetnikova I, Solovchenko A, Khozin-Goldberg I, Cohen Z (2007) Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochloris incisa (Trebouxiophyceae, Chlorophyta). J Phycol 43(4):833–843

    Article  CAS  Google Scholar 

  10. Gong Y, Guo X, Xia W, Zhuo L, Jiang M (2013) Triacylglycerol accumulation and change in fatty acid content of four marine oleaginous microalgae under nutrient limitation and at different culture ages. J Basic Microbiol 53(1):29–36

    Article  CAS  PubMed  Google Scholar 

  11. Chokshi K, Pancha I, Ghosh A, Mishra S (2017) Nitrogen starvation-induced cellular crosstalk of ROS-scavenging antioxidants and phytohormone enhanced the biofuel potential of green microalga Acutodesmus dimorphus. Biotechnol Biofuels 10(1):60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Liu T, Li Y, Liu F, Wang C (2016) The enhanced lipid accumulation in oleaginous microalga by the potential continuous nitrogen-limitation (CNL) strategy. Bioresour Technol 203:150–159

    Article  CAS  PubMed  Google Scholar 

  13. Zhila N, Kalacheva G, Volova T (2005) Influence of nitrogen deficiency on biochemical composition of the green alga Botryococcus. J Appl Phycol 17(4):309–315

    Article  CAS  Google Scholar 

  14. Miller R, Wu G, Deshpande R, Vieler A, Gärtner K, Li X, Moellering E, Zäuner S, Cornish A, Liu B, Bullard B, Sears B, Kuo M, Hegg E, Shachar-Hill Y, Shiu S, Benning C (2010) Changes in transcript abundance in Chlamydomonas reinhardtii following nitrogen deprivation predict diversion of metabolism. Plant Physiol 154(4):1737–1752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Feng P, Deng Z, Fan L, Hu Z (2012) Lipid accumulation and growth characteristics of Chlorella zofingiensis under different nitrate and phosphate concentrations. J Biosci Bioeng 114(4):405–410

    Article  CAS  PubMed  Google Scholar 

  16. Khozin-Goldberg I, Cohen Z (2006) The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus. Phytochemistry 67(7):696–701

    Article  CAS  PubMed  Google Scholar 

  17. Roessler P, Bleibaum J, Thompson G, Ohlrogge J (1994) Characteristics of the gene that encodes acetyl-CoA carboxylase in the diatom Cyclotella cryptica. Ann N Y Acad Sci 721(1):250–256

    Article  CAS  PubMed  Google Scholar 

  18. Sato N, Hagio M, Wada H, Tsuzuki M (2000) Environmental effects on acidic lipids of thylakoid membranes. Biochem Soc Trans 28(6):912–914

    Article  CAS  PubMed  Google Scholar 

  19. Reitan K, Rainuzzo J, Olsen Y (1994) Effect of nutrient limitation on fatty acid and lipid content of marine microalgae. J Phycol 30(6):972–979

    Article  CAS  Google Scholar 

  20. d’Ippolito G, Sardo A, Paris D, Vella F, Adelfi M, Botte P, Gallo C, Fontana A (2015) Potential of lipid metabolism in marine diatoms for biofuel production. Biotechnol Biofuels 8(1):28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Batista I, Garcia A, Van Dalen P, Kamermans P, Verdegem M, Smaal A (2015) Culturing using simplified media with different N sources: effects on production and lipid content. Eur J Phycol 50(1):92–99

    Article  CAS  Google Scholar 

  22. Wang X, Liang J, Luo C, Chen C, Gao Y (2014) Biomass, total lipid production, and fatty acid composition of the marine diatom Chaetoceros muelleri in response to different CO2 levels. Bioresour Technol 161(6):124–130

    CAS  PubMed  Google Scholar 

  23. López-Elías J, Voltolina D, Enríquez-Ocaña F, Gallegossimental G (2005) Indoor and outdoor mass production of the diatom Chaetoceros muelleri in a Mexican commercial hatchery. Aquac Eng 33(3):181–191

    Article  Google Scholar 

  24. Becerra-Dórame M, López-Elías J, Martínez-Córdova L (2010) An alternative outdoor production system for the microalgae Chaetoceros muelleri and Dunaliella sp. during winter and spring in Northwest Mexico. Aquac Eng 43(1):24–28

    Article  Google Scholar 

  25. Hallegraeff G, Anderson D, Cembella A, Enevoldsen H, Commission I (2003) Manual on harmful marine microalgae. UNESCO, Paris

    Google Scholar 

  26. Guillard R (2005) Purification methods for microalgae. In: Andersen RA (ed) Phycological methods: algal culturing techniques. Elsevier Academic Press, Burlington, pp 117–132

    Google Scholar 

  27. Huo S, Zhou W, Wang Z, Zhu S, Dong L, Huang W, Yuan Z, Dong R (2015) Biomass measurement of microalgae cultivated under photoautotrophic conditions for biofuels. Energy Source 37(13):1447–1454

    Article  CAS  Google Scholar 

  28. Tang D, Han W, Li P, Miao X, Zhong J (2011) CO2 biofixation and fatty acid composition of Scenedesmus obliquus and Chlorella pyrenoidosa in response to different CO2 levels. Bioresour Technol 102(3):3071–3076

    Article  CAS  PubMed  Google Scholar 

  29. Jeffrey S, Humphrey G (1975) New spectrophotometric equations for determining chlorophylls a, b, c1 and c2 in higher plants, algae and natural phytoplankton. Biochem Physiol Pflanz 167(19):191–194

    Article  CAS  Google Scholar 

  30. Cooper M, Hardin W, Petersen T, Cattolico R (2010) Visualizing “green oil” in live algal cells. J Biosci Bioeng 109(2):198–201

    Article  CAS  PubMed  Google Scholar 

  31. Dickinson K, Whitney C, Mcginn P (2013) Nutrient remediation rates in municipal wastewater and their effect on biochemical composition of the microalga Scenedesmus sp. AMDD. Algal Res 2(2):127–134

    Article  Google Scholar 

  32. Ishida Y, Hiragushi N, Kitaguchi H, Mitsutani A, Nagai S, Yoshimura M (2000) A highly CO2-tolerant diatom, Thalassiosira weissflogii H1, enriched from coastal sea, and its fatty acid composition. Fish Sci 66(4):655–659

    Article  CAS  Google Scholar 

  33. Miao X, Li R, Yao H (2009) Effective acid-catalyzed transesterification for biodiesel production. Energ Convers Manag 50(10):2680–2684

    Article  CAS  Google Scholar 

  34. Williams P, Laurens L (2010) Microalgae as biodiesel and biomass feedstocks: review and analysis of the biochemistry, energetics and economics. Energ Environ Sci 3(5):554–590

    Article  CAS  Google Scholar 

  35. Singh P, Guldhe A, Kumari S, Rawat I, Bux F (2015) Investigation of combined effect of nitrogen, phosphorus and iron on lipid productivity of microalgae Ankistrodesmus falcatus KJ671624 using response surface methodology. Biochem Eng J 94(42):22–29

    Article  CAS  Google Scholar 

  36. Mansour M, Frampton D, Nichols P, Volkman J, Blackburn S (2005) Lipid and fatty acid yield of nine stationary-phase microalgae: applications and unusual C24–C28 polyunsaturated fatty acids. J Appl Phycol 17(4):287–300

    Article  CAS  Google Scholar 

  37. Bopp S, Lettieri T (2007) Gene regulation in the marine diatom Thalassiosira pseudonana upon exposure to polycyclic aromatic hydrocarbons (PAHs). Gene 396(2):293–302

    Article  CAS  PubMed  Google Scholar 

  38. Chauton M, Olsen Y, Vadstein O (2013) Biomass production from the microalga Phaeodactylum tricornutum: nutrient stress and chemical composition in exponential fed-batch cultures. Biomass Bioenergy 58(6):87–94

    Article  CAS  Google Scholar 

  39. Eizadora T, Zendejas F, Lane P, Gaucher S, Simmons B, Lane T (2009) Triacylglycerol accumulation and profiling in the model diatoms Thalassiosira pseudonana and Phaeodactylum tricornutum (Bacillariophyceae) during starvation. J Appl Phycol 21(6):669–681

    Article  CAS  Google Scholar 

  40. Wu S, Song L, Sommerfeld M, Hu Q, Chen W (2017) Optimization of an effective method for the conversion of crude algal lipids into biodiesel. Fuel 197:467–473

    Article  CAS  Google Scholar 

  41. Hildebrand M, Davis A, Smith S, Traller J, Abbriano R (2012) The place of diatoms in the biofuels industry. Biofuels 3(2):221–240

    Article  CAS  Google Scholar 

  42. Griffiths MJ, Harrison STL (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21(5): 493–507

    Article  CAS  Google Scholar 

  43. Butterwick C, Heaney SI, Talling JF (2005) Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshwater Biol 50(2): 291–300

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National 973 project under Grant number 2011CB200901, and the National Natural Science Foundation of China (Grant nos. 41576138 and 41276130).

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Authors and Affiliations

  1. School of Pharmaceutical Sciences, Xiamen University, Xiamen, 361102, China

    Qun Lin

  2. School of Life Sciences, Xiamen University, Xiamen, 361102, China

    Qun Lin, Wen-Hao Zhuo, Xin-Wei Wang, Chang-Ping Chen, Ya-Hui Gao & Jun-Rong Liang

  3. Key Laboratory of the Coastal and Wetland Ecosystems (Xiamen University), Ministry of Education, Xiamen, 361102, China

    Chang-Ping Chen & Jun-Rong Liang

  4. State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361102, China

    Ya-Hui Gao

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  1. Qun Lin
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Correspondence to Jun-Rong Liang.

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Lin, Q., Zhuo, WH., Wang, XW. et al. Effects of fundamental nutrient stresses on the lipid accumulation profiles in two diatom species Thalassiosira weissflogii and Chaetoceros muelleri. Bioprocess Biosyst Eng 41, 1213–1224 (2018). https://doi.org/10.1007/s00449-018-1950-z

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