Advertisement

Journal of Applied Phycology

, Volume 30, Issue 4, pp 2237–2246 | Cite as

Simultaneous increase in cellular content and volumetric concentration of lipids in Bracteacoccus bullatus cultivated at reduced nitrogen and phosphorus concentrations

  • Anna Mamaeva
  • Zorigto Namsaraev
  • Yevhen Maltsev
  • Evgeniy Gusev
  • Maxim Kulikovskiy
  • Maria Petrushkina
  • Alla Filimonova
  • Boris Sorokin
  • Nikita Zotko
  • Vladimir Vinokurov
  • Dmitry Kopitsyn
  • Daria Petrova
  • Andrei Novikov
  • Denis Kuzmin
Article

Abstract

Manipulation of the nutrient concentration is an inexpensive and efficient method for increasing lipid and TAG accumulation in algal cells. However, high volumetric production requires finding a proper balance between the decrease of biomass production and the increase in the total lipid content. We isolated a strain of green microalga Bracteacoccus bullatus and increased its lipid content from 17 to 59% of biomass dry weight by manipulating of nitrogen and phosphorus content in the medium. The 10-fold reduction of the nitrogen and phosphorus concentration in the medium was the most efficient method of the lipid induction compared to nutrient deplete and high nutrient conditions. The oleic (48–64% mass of total fatty acids) and linoleic (14–24% mass of total fatty acids) acids dominated in the fatty acid profile, thus making this strain a suitable candidate for biodiesel production.

Keywords

Chlorophyta Lipids Triacylglycerides (TAGs) Fatty acid Nitrogen and phosphorus deprivation 

Notes

Acknowledgements

All authors contributed equally to this work. In general, LLC “Solixant” is interested in the potential of microalgae as an alternative sustainable source of lipids. This does not alter the authors’ adherence to the Journal of Applied Phycology policies on sharing data and materials. This work was supported by Ministry of Education and Science of the Russian Federation (project 14.574.21.0137, identifier RFMEFI57417X0137).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefPubMedGoogle Scholar
  2. Bona F, Capuzzo A, Franchino M, Maffei ME (2014) Semicontinuous nitrogen limitation as convenient operation strategy to maximize fatty acid production in Neochloris oleoabundans. Algal Res 5:1–6CrossRefGoogle Scholar
  3. 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 124:217–226CrossRefPubMedGoogle Scholar
  4. Broady PA (1984) Taxonomic and ecological investigations of algae on steam-warmed soil on Mt. Erebus, Ross Island, Antarctica. Phycologia 23:257–271CrossRefGoogle Scholar
  5. Byun Y, Han K (2009) PseudoViewer3: generating planar drawings of large-scale RNA structures with pseudoknots. Bioinformatics 25:1435–1437CrossRefPubMedGoogle Scholar
  6. Caisová L, Marin B, Melkonian M (2013) A consensus secondary structure of ITS2 in the Chlorophyta identified by phylogenetic reconstruction. Protist 164:482–496CrossRefPubMedGoogle Scholar
  7. Challagulla V, Fabbro L, Nayar S (2015) Biomass, lipid productivity and fatty acid composition of fresh water microalga Rhopalosolen saccatus cultivated under phosphorus limited conditions. Algal Res 8:69–75CrossRefGoogle Scholar
  8. Chen W, Zhang CH, Song L, Sommerfeld M, Hu Q (2009) A high throughput Nile Red method for quantitative measurement of neutral lipids in microalgae. J Microbiol Methods 77:41–47CrossRefPubMedGoogle Scholar
  9. Coleman AW (2003) ITS2 is a double-edged tool for eukaryote evolutionary comparisons. Trends Genet 19:370–375CrossRefPubMedGoogle Scholar
  10. Dodds ED, McCoy MR, Rea LD, Kennish JM (2005) Gas chromatographic quantification of fatty acid methyl esters: flame ionization detection vs. electron impact mass spectrometry. Lipids 40:419–428CrossRefPubMedGoogle Scholar
  11. Fields MW, Hise A, Lohman EJ, Bell T, Gardner RD, Corredor L, Moll K, Peyton BM, Characklis GW, Gerlach R (2014) Sources and resources: importance of nutrients, resource allocation, and ecology in microalgal cultivation for lipid accumulation. Appl Microbiol Biotechnol 98:4805–4816CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fučíková K, Flechtner VR, Lewis LA (2012) Revision of the genus Bracteacoccus Tereg (Chlorophyceae, Chlorophyta) based on a phylogenetic approach. Nova Hedwigia 96:15–59CrossRefGoogle Scholar
  13. Goncalves EC, Wilkie AC, Kirst M, Rathinasabapathi B (2016) Metabolic regulation of triacylglycerol accumulation in the green algae: identification of potential targets for engineering to improve oil yield. Plant Biotechnol J 14:1649–1660CrossRefPubMedPubMedCentralGoogle Scholar
  14. Griffiths MJ, Harrison STL (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507CrossRefGoogle Scholar
  15. Guillard RR, Lorenzen CJ (1972) Yellow-green algae with chlorophyllide c. J Phycol 8:10–14Google Scholar
  16. Guschina IA, Harwood JL (2013) Algal lipids and their metabolism. In: Borowitzka MA, Moheimani NR (eds) Algae for Biofuels and Energy. Springer, Dordrecht, pp 17–36CrossRefGoogle Scholar
  17. 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 54:621–639CrossRefPubMedGoogle Scholar
  18. Katoh K, Toh H (2010) Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26:1899–1900CrossRefPubMedPubMedCentralGoogle Scholar
  19. Keller A, Schleicher T, Förster F, Ruderisch B, Dandekar T, Müller T, Wolf M (2008) ITS2 data corroborate a monophyletic chlorophycean DO-group (Sphaeropleales). BMC Evol Biol 8:218CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 67:696–701CrossRefPubMedGoogle Scholar
  21. Koetschan C, Förster F, Keller A, Schleicher T, Ruderisch B, Schwarz R, Müller T, Wolf M, Schultz J (2010) The ITS2 Database III—sequences and structures for phylogeny. Nucleic Acids Res 38:D275–D279CrossRefPubMedGoogle Scholar
  22. Kumar MS, Ramesh A, Nagalingam B (2003) An experimental comparison of methods to use methanol and Jatropha oil in a compression ignition engine. Biomass Bioenergy 25:309–318CrossRefGoogle Scholar
  23. 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 81:629–636CrossRefPubMedGoogle Scholar
  24. 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
  25. Lv JM, Cheng LH, Xu XH, Zhang L, Chen HL (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101:6797–6804CrossRefPubMedGoogle Scholar
  26. Maltsev YI, Konovalenko TV, Barantsova IA, Maltseva IA, Maltseva KI (2017a) Prospects of using algae in biofuel production. Regul Mech Biosyst 8:455–460CrossRefGoogle Scholar
  27. Maltsev YI, Pakhomov AY, Maltseva IA (2017b) Specific features of algal communities in forest litter of forest biogeocenoses of the steppe zone. Contemp Probl Ecol 10:71–76CrossRefGoogle Scholar
  28. Maltseva IA, Maltsev YI, Solonenko AN (2017) Soil algae of the oak groves of the steppe zone of Ukraine. Int J Algae 19:215–226CrossRefGoogle Scholar
  29. Mandal S, Mallick N (2009) Microalga Scenedesmus obliquus as a potential source for biodiesel production. Appl Microbiol Biotechnol 84:281–291CrossRefPubMedGoogle Scholar
  30. Mansour MP, Frampton DMF, Nichols PD, Volkman JK, Blackburn SI (2005) Lipid and fatty acid yield of nine stationary-phase microalgae: applications and unusual C24–C28 polyunsaturated fatty acids. J Appl Phycol 17:287–300CrossRefGoogle Scholar
  31. Minyuk GS, Chelebieva ES, Chubchikova IN (2015) Secondary carotenogenesis of the green microalga Bracteacoccus minor (Chlorophyta) in a two-stage culture. Int J Algae 25:21–34Google Scholar
  32. Patova EN, Dorokhova MF (2008) Green algae in tundra soils affected by coal mine pollutions. Biologia 63:831–835CrossRefGoogle Scholar
  33. Posada D (2006) Modeltest server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:700–703CrossRefGoogle Scholar
  34. Ratha SK, Babu S, Renuka N, Prasanna R, Prasad RBN, Saxena AK (2012) Exploring nutritional modes of cultivation for enhancing lipid accumulation in microalgae. J Basic Microbiol 53:440–450CrossRefPubMedGoogle Scholar
  35. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  36. Scherbina VV, Maltseva IA, Solonenko AN (2014) Peculiarities of postpyrogene development of algae in steppe biocenoses at Askania Nova Biospheric national park. Contemp Probl Ecol 7:187–191CrossRefGoogle Scholar
  37. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 57:758–771CrossRefPubMedGoogle Scholar
  38. Talebi AF, Mohtashami SK, Tabatabaei M, Tohidfar M, Bagheri A, Zeinalabedini М, 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. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  40. Wan C, Bai FW, Zhao XQ (2013) Effects of nitrogen concentration and media replacement on cell growth and lipid production of oleaginous marine microalga Nannochloropsis oceanica DUT01. Biochem Eng J 78:32–38CrossRefGoogle Scholar
  41. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  42. Zhang S, Liu PH, Yang X, Hao ZD, Zhang L, Luo N, Shi J (2014) Isolation and identification by 18S rDNA sequence of high lipid potential microalgal species for fuel production in Hainan Dao. Biomass Bioenergy 66:197–203CrossRefGoogle Scholar
  43. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Anna Mamaeva
    • 1
  • Zorigto Namsaraev
    • 2
  • Yevhen Maltsev
    • 3
    • 4
  • Evgeniy Gusev
    • 1
    • 5
  • Maxim Kulikovskiy
    • 5
  • Maria Petrushkina
    • 1
    • 6
  • Alla Filimonova
    • 1
  • Boris Sorokin
    • 1
    • 6
  • Nikita Zotko
    • 1
  • Vladimir Vinokurov
    • 6
  • Dmitry Kopitsyn
    • 6
  • Daria Petrova
    • 6
  • Andrei Novikov
    • 6
  • Denis Kuzmin
    • 1
  1. 1.LLC “Solixant”MoscowRussia
  2. 2.NRC “Kurchatov Institute”MoscowRussia
  3. 3.Papanin Institute for Biology of Inland Waters RASBorokRussia
  4. 4.Bohdan Khmelnytskyi Melitopоl State Pedagogical UniversityMelitopolUkraine
  5. 5.Timiryazev Institute of Plant Physiology RASMoscowRussia
  6. 6.Gubkin Russian State University of Oil and GasMoscowRussia

Personalised recommendations