Advertisement

Differential carbon partitioning and fatty acid composition in mixotrophic and autotrophic cultures of a new marine isolate Tetraselmis sp. KY114885

  • Zahra Lari
  • Parvaneh Abrishamchi
  • Hossein Ahmadzadeh
  • Neda Soltani
Article
First Online:
Received:
Revised:
Accepted:

Abstract

Biochemical composition of microalgae, a promising feedstock for biodiesel production, can be modified under different nutritional modes. The objective of this study was to investigate the influence of autotrophy and mixotrophy on the growth and biochemical composition of Tetraselmis sp. KY114885. Time-course variations of lipids and starch were determined using gravimetric and colorimetric methods. After direct transesterification, lipid profile on days 12 and 20 of cultivation period was determined. The results revealed higher growth of microalgae in mixotrophic cultures containing 5 g L−1 glucose, whereas 7.5 g L−1 glucose suppressed growth. Mixotrophy enhanced the lipid and starch yields in a distinctive trend. The fatty acid composition changed with the different nutritional regimes and the length of growth in batch culture. Glucose supplementation elevated the portions of monounsaturated fatty acids, particularly oleic acid, and decreased the percentage of saturated and polyunsaturated fatty acids. The present study suggests that mixotrophic cultivation of Tetraselmis sp. KY114885 may be a feasible strategy to improve growth parameters and the biochemical composition of the alga for biofuel production. The results also shed light on carbon allocation in the algae grown under two different trophic modes.

Keywords

Chlorophyta Microalgae Mixotrophy Glucose Lipid Starch 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

The authors acknowledge Research Institute for Applied Sciences, Academic Center for Education, Culture and Research (ACECR), Tehran, for providing the alga and molecular identification of the strain.

Funding information

Financial support was provided by Ferdowsi University of Mashhad (grant no. 3/27412).

References

  1. Baldisserotto C, Popovich C, Giovanardi M, Sabia A, Ferroni L, Constenla D, Leonardi P, Pancaldi S (2016) Photosynthetic aspects and lipid profiles in the mixotrophic alga Neochloris oleoabundans as useful parameters for biodiesel production. Algal Res 16:255–265Google Scholar
  2. Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv 32:1476–1493CrossRefPubMedGoogle Scholar
  3. Benemann J (2013) Microalgae for biofuels and animal feeds. Energies 6:5869–5886CrossRefGoogle Scholar
  4. Borowitzka MA (2013) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756CrossRefGoogle Scholar
  5. Cheng D, Li D, Yuan Y, Zhou L, Li X, Wu T, Wang L, Zhao Q, Wei W, Sun Y (2017) Improving carbohydrate and starch accumulation in Chlorella sp. AE10 by a novel two-stage process with cell dilution. Biotechnol Biofuels 10(1):75CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cid A, Abalde J, Herrero C (1992) High yield mixotrophic cultures of the marine microalga Tetraselmis suecica (Kylin) Butcher (Prasinophyceae). J Appl Phycol 4:31–37CrossRefGoogle Scholar
  7. Cheirsilp B, Torpee S (2012) Enhanced growth and lipid production of microalgae under mixotrophic culture condition: Effect of light intensity, glucose concentration and fed-batch cultivation. Bioresour Technol 110:510–516CrossRefPubMedGoogle Scholar
  8. de Jaeger L, Verbeek RE, Draaisma RB, Martens DE, Springer J, Eggink G, Wijffels RH (2014) Superior triacylglycerol (TAG) accumulation in starchless mutants of Scenedesmus obliquus:(I) Mutant generation and characterization. Biotechnol Biofuels 7(1):69CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fon-Sing S, Borowitzka M (2016) Isolation and screening of euryhaline Tetraselmis spp. suitable for large-scale outdoor culture in hypersaline media for biofuels. J Appl Phycol 28:1–14CrossRefGoogle Scholar
  10. Guillard RRL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith WL, Chanley MH (eds) Culture of marine invertebrate animals. Plenum Press, New York, pp 29–60CrossRefGoogle Scholar
  11. Haass D, Tanner W (1974) Regulation of hexose transport in Chlorella vulgaris. Characteristics of induction and turnover. Plant Physiol 53:14–20CrossRefPubMedPubMedCentralGoogle Scholar
  12. Jia J, Han D, Gerken HG, Li Y, Sommerfeld M, Hu Q, Xu J (2015) Molecular mechanisms for photosynthetic carbon partitioning into storage neutral lipids in Nannochloropsis oceanica under nitrogen-depletion conditions. Algal Res 7:66–77CrossRefGoogle Scholar
  13. Knothe G (2006) Analyzing biodiesel: standards and other methods. JAOAC 83:823–833Google Scholar
  14. Kong W-B, Hua S-F, Cao H, Mu Y-W, Yang H, Song H, Xia C-G (2012) Optimization of mixotrophic medium components for biomass production and biochemical composition biosynthesis by Chlorella vulgaris using response surface methodology. J Taiwan Inst Chem Eng 43(3):360–367CrossRefGoogle Scholar
  15. Kong W-B, Yang H, Cao Y-T, Song H, Hua S-F, Xia C-G (2013) Effect of glycerol and glucose on the enhancement of biomass, lipid and soluble carbohydrate production by Chlorella vulgaris in mixotrophic culture. Food Technol Biotechnol 51:62–69Google Scholar
  16. Krzemińska I, Oleszek M (2016) Glucose supplementation-induced changes in the Auxenochlorella protothecoides fatty acid composition suitable for biodiesel production. Bioresour Technol 218:1294–1297CrossRefPubMedGoogle Scholar
  17. Li T, Gargouri M, Feng J, Park J-J, Gao D, Miao C, Dong T, Gang DR, Chen S (2015) Regulation of starch and lipid accumulation in a microalga Chlorella sorokiniana. Bioresour Technol 180:250–257CrossRefPubMedGoogle Scholar
  18. Li T, Zheng Y, Yu L, Chen S (2014) Mixotrophic cultivation of a Chlorella sorokiniana strain for enhanced biomass and lipid production. Biomass Bioenergy 66:204–213CrossRefGoogle Scholar
  19. 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 102:123–129CrossRefPubMedGoogle Scholar
  20. Lu L, Wang J, Yang G, Zhu B, Pan K (2017a) Biomass and nutrient productivities of Tetraselmis chuii under mixotrophic culture conditions with various C:N ratios. Chin J Oceanol 35(2):303–312Google Scholar
  21. Lu L, Wang J, Yang G, Zhu B, Pan K (2017b) Heterotrophic growth and nutrient productivities of Tetraselmis chuii using glucose as a carbon source under different C/N ratios. J Appl Phycol 29:15–21Google Scholar
  22. Milledge JJ (2011) Commercial application of microalgae other than as biofuels: a brief review. Rev Env Sci Bio/Tech 10(1):31–41CrossRefGoogle Scholar
  23. Mizuno Y, Sato A, Watanabe K, Hirata A, Takeshita T, Ota S, Sato N, Zachleder V, Tsuzuki M, Kawano S (2013) Sequential accumulation of starch and lipid induced by sulfur deficiency in Chlorella and Parachlorella species. Bioresour Technol 129:150–155CrossRefPubMedGoogle Scholar
  24. Mohamed MS, Tan JS, Kadkhodaei S, Mohamad R, Mokhtar MN, Ariff AB (2014) Kinetics and modeling of microalga Tetraselmis sp. FTC 209 growth with respect to its adaptation toward different trophic conditions. Biochem Eng J 88:30–41CrossRefGoogle Scholar
  25. Mohan SV, Rohit M, Chiranjeevi P, Chandra R, Navaneeth B (2015) Heterotrophic microalgae cultivation to synergize biodiesel production with waste remediation: progress and perspectives. Bioresour Technol 184:169–178CrossRefGoogle Scholar
  26. Moheimani NR (2013) Inorganic carbon and pH effect on growth and lipid productivity of Tetraselmis suecica and Chlorella sp (Chlorophyta) grown outdoors in bag photobioreactors. J Appl Phycol 25:387–398CrossRefGoogle Scholar
  27. Morales-Sánchez D, Tinoco-Valencia R, Kyndt J, Martinez A (2013) Heterotrophic growth of Neochloris oleoabundans using glucose as a carbon source. Biotechnol Biofuels 6(1):100CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ngangkham M, Ratha SK, Prasanna R, Saxena AK, Dhar DW, Sarika C, Prasad RBN (2012) Biochemical modulation of growth, lipid quality and productivity in mixotrophic cultures of Chlorella sorokiniana. SpringerPlus 1(1):33CrossRefPubMedPubMedCentralGoogle Scholar
  29. Park KC, Whitney C, McNichol JC, Dickinson KE, MacQuarrie S, Skrupski BP, Zou J, Wilson KE, O’Leary SJ, McGinn PJ (2012) Mixotrophic and photoautotrophic cultivation of 14 microalgae isolates from Saskatchewan, Canada: potential applications for wastewater remediation for biofuel production. J Appl Phycol 24:339–348CrossRefGoogle Scholar
  30. Reed MC, Lieb A, Nijhout HF (2010) The biological significance of substrate inhibition: a mechanism with diverse functions. Bioessays 32:422–429CrossRefPubMedGoogle Scholar
  31. Ren X, Chen J, Deschênes J-S, Tremblay R, Jolicoeur M (2016) Glucose feeding recalibrates carbon flux distribution and favours lipid accumulation in Chlorella protothecoides through cell energetic management. Algal Res 14:83–91CrossRefGoogle Scholar
  32. Sabia A, Baldisserotto C, Biondi S, Marchesini R, Tedeschi P, Maietti A, Giovanardi M, Ferroni L, Pancaldi S (2015) Re-cultivation of Neochloris oleoabundans in exhausted autotrophic and mixotrophic media: the potential role of polyamines and free fatty acids. Appl Microbiol Biotechnol 99:10597–10609Google Scholar
  33. Selvakumar P, Umadevi K (2014) Enhanced lipid and fatty acid content under photoheterotrophic condition in the mass cultures of Tetraselmis gracilis and Platymonas convolutae. Algal Res 6:180–185CrossRefGoogle Scholar
  34. Shishlyannikov SM, Klimenkov IV, Bedoshvili YD, Mikhailov IS, Gorshkov AG (2014) Effect of mixotrophic growth on the ultrastructure and fatty acid composition of the diatom Synedra acus from Lake Baikal. J Biol Res Thessaloniki 21(1):15CrossRefGoogle Scholar
  35. Sing SF, Isdepsky A, Borowitzka M, Lewis D (2014) Pilot-scale continuous recycling of growth medium for the mass culture of a halotolerant Tetraselmis sp. in raceway ponds under increasing salinity: a novel protocol for commercial microalgal biomass production. Bioresour Technol 161:47–54CrossRefGoogle Scholar
  36. Smith RT, Bangert K, Wilkinson SJ, Gilmour DJ (2015) Synergistic carbon metabolism in a fast growing mixotrophic freshwater microalgal species Micractinium inermum. Biomass Bioenergy 82:73–86CrossRefGoogle Scholar
  37. Subramanian S, Barry AN, Pieris S, Sayre RT (2013) Comparative energetics and kinetics of autotrophic lipid and starch metabolism in chlorophytic microalgae: implications for biomass and biofuel production. Biotechnol Biofuels 6(1):150CrossRefPubMedPubMedCentralGoogle Scholar
  38. Talebi AF, Mohtashami SK, Tabatabaei M, Tohidfar M, Bagheri A, Zeinalabedini M, Mirzaei HH, Mirzajanzadeh M, Shafaroudi SM, Bakhtiari S (2013) Fatty acids profiling: a selective criterion for screening microalgae strains for biodiesel production. Algal Res 2:258–267CrossRefGoogle Scholar
  39. Vitova M, Bisova K, Kawano S, Zachleder V (2015) Accumulation of energy reserves in algae: from cell cycles to biotechnological applications. Biotechnol Adv 33:1204–1218CrossRefPubMedGoogle Scholar
  40. Yeh K-L, Chang J-S (2012) Effects of cultivation conditions and media composition on cell growth and lipid productivity of indigenous microalga Chlorella vulgaris ESP-31. Bioresour Technol 105:120–127CrossRefPubMedGoogle Scholar
  41. Zhao G, Yu J, Jiang F, Zhang X, Tan T (2012) The effect of different trophic modes on lipid accumulation of Scenedesmus quadricauda. Bioresour Technol 114:466–471Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Zahra Lari
    • 1
  • Parvaneh Abrishamchi
    • 1
  • Hossein Ahmadzadeh
    • 2
  • Neda Soltani
    • 3
  1. 1.Department of Biology, Faculty of ScienceFerdowsi University of MashhadMashhadIran
  2. 2.Department of Chemistry, Faculty of ScienceFerdowsi University of MashhadMashhadIran
  3. 3.Department of Petroleum MicrobiologyResearch Institute of Applied ScienceTehranIran

Personalised recommendations