Cited by 245Algal biology and biofuel productionMicrobial Metabolic Engineering and BioproductionLipid metabolism and biosynthesis

Strategies for Lipid Production Improvement in Microalgae as a Biodiesel Feedstock

Open access
Zhu, L. D., Li, Z. H., Hiltunen, E.·2016·BioMed Research International

Abstract

In response to the energy crisis, global warming, and climate changes, microalgae have received a great deal of attention as a biofuel feedstock. Due to a high lipid content in microalgal cells, microalgae present as a promising alternative source for the production of biodiesel. Environmental and culturing condition variations can alter lipid production as well as chemical compositions of microalgae. Therefore, application of the strategies to activate lipid accumulation opens the door for lipid overproduction in microalgae. Until now, many original studies regarding the approaches for enhanced microalgal lipid production have been reported in an effort to push forward the production of microalgal biodiesel. However, the current literature demonstrates fragmented information available regarding the strategies for lipid production improvement. From the systematic point of view, the review highlights the main approaches for microalgal lipid accumulation induction to expedite the application of microalgal biodiesel as an alternative to fossil diesel for sustainable environment. Of the several strategies discussed, the one that is most commonly applied is the design of nutrient (e.g., nitrogen, phosphorus, and sulfur) starvation or limitation. Other viable approaches such as light intensity, temperature, carbon dioxide, salinity stress, and metal influence can also achieve enhanced microalgal lipid production.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1155/2016/8792548

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • pH, salinity, and mineral salts are major stimuli affecting lipid production.

    “Besides these factors, pH, salinity, and mineral salts are also major stimuli affecting lipid production (Zhu et al. 2016).”

    From Production of microalgae with high lipid content and their potential as sources of nutraceuticals (2023) · cites this paper as Zhu et al. 2016

    Section 3.5 (Salinity Stress; page unavailable) reports that salinity stress can increase microalgal lipid content, and section 3.6 (Metal Stress; page unavailable) reports effects of mineral ions on lipid production. Section 3.3 (Carbon Dioxide; page unavailable) mentions pH only as a consequence of excess CO2; it does not identify pH itself as a major stimulus affecting lipid production. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 65 · Cited by 245

Research works printed but not linked: 61

  1. [1]Langholtz M. H. Coleman A. M. Eaton L. M. Wigmosta M. S. Hellwinckel C. M. Brandt C. C. Potential land competition between open-pond microalgae production and terrestrial dedicated feedstock supply systems in the U.S. Renewable Energy 2016 93 201 214 10.1016/j.renene.2016.02.052 · DOI
  2. [2]Gunatilake H. Roland-Holst D. Sugiyarto G. Energy security for India: biofuels, energy efficiency and food productivity Energy Policy 2014 65 761 767 10.1016/j.enpol.2013.10.050 2-s2.0-84890315389 · DOI
  3. [3]Zhu L. Huo S. Qin L. A microalgae-based biodiesel refinery: sustainability concerns and challenges International Journal of Green Energy 2015 12 6 595 602 10.1080/15435075.2013.867406 2-s2.0-84924750358 · DOI · Paper page
  4. [4]Chanthawong A. Dhakal S. Stakeholders' perceptions on challenges and opportunities for biodiesel and bioethanol policy development in Thailand Energy Policy 2016 91 189 206 10.1016/j.enpol.2016.01.008 2-s2.0-84958246240 · DOI
  5. [5]Zhu L. Microalgal culture strategies for biofuel production: a review Biofuels, Bioproducts and Biorefining 2015 9 6 801 814 10.1002/bbb.1576 2-s2.0-84954385953 · DOI
  6. [6]Zhu L. Shuhao H. Shakeel S. Li Z. Algal biorefinery for sustainable development and the challenges Proceedings of the Institution of Civil Engineers—Energy 2016 10.1680/jener.16.00001 · DOI
  7. [7]Han F. Pei H. Hu W. Jiang L. Cheng J. Zhang L. Beneficial changes in biomass and lipid of microalgae Anabaena variabilis facing the ultrasonic stress environment Bioresource Technology 2016 209 16 22 10.1016/j.biortech.2016.02.103 26946436 · DOI
  8. [8]Zhu L. The combined production of ethanol and biogas from microalgal residuals to sustain microalgal biodiesel: a theoretical evaluation Biofuels, Bioproducts and Biorefining 2014 8 1 7 15 10.1002/bbb.1442 2-s2.0-84892480873 · DOI
  9. [9]Medipally S. R. Yusoff F. M. Banerjee S. Shariff M. Microalgae as sustainable renewable energy feedstock for biofuel production BioMed Research International 2015 2015 13 519513 10.1155/2015/519513 2-s2.0-84927154665 PMC4385614 25874216 · DOI · Paper page
  10. [10]Zhu L. Biorefinery as a promising approach to promote microalgae industry: an innovative framework Renewable and Sustainable Energy Reviews 2015 41 1376 1384 10.1016/j.rser.2014.09.040 2-s2.0-84908424375 · DOI · Paper page
  11. [11]Vitova M. Bisova K. Kawano S. Zachleder V. Accumulation of energy reserves in algae: from cell cycles to biotechnological applications Biotechnology Advances 2015 33 6 1204 1218 10.1016/j.biotechadv.2015.04.012 2-s2.0-84955191764 25986035 · DOI
  12. [12]Zhu L. D. Xu Z. B. Qin L. Wang Z. M. Hiltunen E. Li Z. H. Oil production from pilot-scale microalgae cultivation: an economics evaluation Energy Sources, Part B: Economics, Planning, and Policy 2016 11 1 11 17 10.1080/15567249.2015.1052594 · DOI
  13. [13]Berg A. H. Combs T. P. Scherer P. E. ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism Trends in Endocrinology & Metabolism 2002 13 2 84 89 10.1016/s1043-2760(01)00524-0 2-s2.0-0036511213 11854024 · DOI
  14. [14]de Jaeger L. Verbeek R. E. M. Draaisma R. B. Superior triacylglycerol (TAG) accumulation in starchless mutants of Scenedesmus obliquus: (I) mutant generation and characterization Biotechnology for Biofuels 2014 7 1, article 69 10.1186/1754-6834-7-69 2-s2.0-84902544697 PMC4052810 24920957 · DOI
  15. [15]Bišová K. Zachleder V. Cell-cycle regulation in green algae dividing by multiple fission Journal of Experimental Botany 2014 65 10 2585 2602 10.1093/jxb/ert466 2-s2.0-84902370355 24441762 · DOI
  16. [16]Wang Z. T. Ullrich N. Joo S. Waffenschmidt S. Goodenough U. Algal lipid bodies: stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii Eukaryotic Cell 2009 8 12 1856 1868 10.1128/ec.00272-09 2-s2.0-73349097525 19880756 PMC2794211 · DOI
  17. [17]Li Y. T. Han D. X. Hu G. R. Sommerfeld M. Hu Q. A. Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii Biotechnology and Bioengineering 2010 107 2 258 268 10.1002/bit.22807 2-s2.0-77956825813 20506159 · DOI
  18. [18]Li Y. Han D. Hu G. Chlamydomonas starchless mutant defective in ADP-glucose pyrophosphorylase hyper-accumulates triacylglycerol Metabolic Engineering 2010 12 4 387 391 10.1016/j.ymben.2010.02.002 2-s2.0-77953023710 20172043 · DOI
  19. [19]Hallenbeck P. C. Grogger M. Mraz M. Veverka D. The use of Design of Experiments and Response Surface Methodology to optimize biomass and lipid production by the oleaginous marine green alga, Nannochloropsis gaditana in response to light intensity, inoculum size and CO2 Bioresource Technology 2015 184 161 168 10.1016/j.biortech.2014.09.022 2-s2.0-84939980348 25304731 · DOI
  20. [22]Takeshita T. Ota S. Yamazaki T. Hirata A. Zachleder V. Kawano S. Starch and lipid accumulation in eight strains of six Chlorella species under comparatively high light intensity and aeration culture conditions Bioresource Technology 2014 158 127 134 10.1016/j.biortech.2014.01.135 2-s2.0-84896892707 24583913 · DOI
  21. [23]Mandotra S. K. Kumar P. Suseela M. R. Nayaka S. Ramteke P. W. Evaluation of fatty acid profile and biodiesel properties of microalga Scenedesmus abundans under the influence of phosphorus, pH and light intensities Bioresource Technology 2016 201 222 229 10.1016/j.biortech.2015.11.042 2-s2.0-84949293265 26675046 · DOI
  22. [24]Yeesang C. Cheirsilp B. 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 Bioresource Technology 2011 102 3 3034 3040 10.1016/j.biortech.2010.10.013 2-s2.0-78650805539 20980142 · DOI
  23. [25]Sun X. Cao Y. Xu H. Effect of nitrogen-starvation, light intensity and iron on triacylglyceride/carbohydrate production and fatty acid profile of Neochloris oleoabundans HK-129 by a two-stage process Bioresource Technology 2014 155 204 212 10.1016/j.biortech.2013.12.109 2-s2.0-84892844969 24457305 · DOI
  24. [26]Zhu L.-D. Hiltunen E. Methylation of DACT2 accelerates esophageal cancer development by activating Wnt signaling Renewable and Sustainable Energy Reviews 2016 54 1285 1290 10.1016/j.rser.2015.10.093 2-s2.0-84946600345 · DOI
  25. [28]Converti A. Casazza A. A. Ortiz E. Y. Perego P. Del Borghi M. Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production Chemical Engineering and Processing: Process Intensification 2009 48 6 1146 1151 10.1016/j.cep.2009.03.006 2-s2.0-66849112031 · DOI · Paper page
  26. [29]Xin L. Hong-ying H. Yu-ping Z. Growth and lipid accumulation properties of a freshwater microalga Scenedesmus sp. under different cultivation temperature Bioresource Technology 2011 102 3 3098 3102 10.1016/j.biortech.2010.10.055 2-s2.0-78650802614 21055924 · DOI
  27. [30]Cao J. Yuan H. Li B. Yang J. Significance evaluation of the effects of environmental factors on the lipid accumulation of Chlorella minutissima UTEX 2341 under low-nutrition heterotrophic condition Bioresource Technology 2014 152 177 184 10.1016/j.biortech.2013.10.084 2-s2.0-84888404760 24291318 · DOI
  28. [31]Wei L. Huang X. Huang Z. Temperature effects on lipid properties of microalgae Tetraselmis subcordiformis and Nannochloropsis oculata as biofuel resources Chinese Journal of Oceanology and Limnology 2015 33 1 99 106 10.1007/s00343-015-3346-0 2-s2.0-84920572998 · DOI · Paper page
  29. [32]James G. O. Hocart C. H. Hillier W. Price G. D. Djordjevic M. A. Temperature modulation of fatty acid profiles for biofuel production in nitrogen deprived Chlamydomonas reinhardtii Bioresource Technology 2013 127 441 447 10.1016/j.biortech.2012.09.090 2-s2.0-84868305840 23138068 · DOI
  30. [33]Li X. Přibyl P. Bišová K. The microalga Parachlorella kessleri—a novel highly efficient lipid producer Biotechnology and Bioengineering 2013 110 1 97 107 10.1002/bit.24595 2-s2.0-84869863874 22766749 · DOI
  31. [34]Gardner R. D. Lohman E. Gerlach R. Cooksey K. E. Peyton B. M. Comparison of CO2 and bicarbonate as inorganic carbon sources for triacylglycerol and starch accumulation in Chlamydomonas reinhardtii Biotechnology and Bioengineering 2013 110 1 87 96 10.1002/bit.24592 2-s2.0-84869890055 22767335 · DOI
  32. [36]Widjaja A. Chien C.-C. Ju Y.-H. Study of increasing lipid production from fresh water microalgae Chlorella vulgaris Journal of the Taiwan Institute of Chemical Engineers 2009 40 1 13 20 10.1016/j.jtice.2008.07.007 2-s2.0-58249126028 · DOI
  33. [39]Ho S.-H. Chen C.-Y. Chang J.-S. Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N Bioresource Technology 2012 113 244 252 10.1016/j.biortech.2011.11.133 2-s2.0-84860246501 22209130 · DOI
  34. [40]Breuer G. Lamers P. P. Martens D. E. Draaisma R. B. Wijffels R. H. Effect of light intensity, pH, and temperature on triacylglycerol (TAG) accumulation induced by nitrogen starvation in Scenedesmus obliquus Bioresource Technology 2013 143 1 9 10.1016/j.biortech.2013.05.105 2-s2.0-84879308946 23774290 · DOI · Paper page
  35. [41]Zhu L. D. Takala J. Hiltunen E. Wang Z. M. Recycling harvest water to cultivate Chlorella zofingiensis under nutrient limitation for biodiesel production Bioresource Technology 2013 144 14 20 10.1016/j.biortech.2013.06.061 2-s2.0-84880338331 23850821 · DOI
  36. [42]Li Y. Han F. Xu H. Potential lipid accumulation and growth characteristic of the green alga Chlorella with combination cultivation mode of nitrogen (N) and phosphorus (P) Bioresource Technology 2014 174 24 32 10.1016/j.biortech.2014.09.142 2-s2.0-84908273020 25463778 · DOI
  37. [43]Brányiková I. Maršálková B. Doucha J. Microalgae-novel highly efficient starch producers Biotechnology and Bioengineering 2011 108 4 766 776 10.1002/bit.23016 2-s2.0-79952599027 21404251 · DOI
  38. [44]Alabi A. O. Tampier M. Bibeau E. Microalgae technologies and processes for biofuels/bioenergy production in British Columbia Current Technology, Suitability and Barriers to Implementation. Final Report 2009 The British Columbia Innovation Council. Seed Science Press
  39. [45]Ito T. Tanaka M. Shinkawa H. Metabolic and morphological changes of an oil accumulating trebouxiophycean alga in nitrogen-deficient conditions Metabolomics 2013 9 1 178 187 10.1007/s11306-012-0463-z 2-s2.0-84874355250 23463323 PMC3580136 · DOI
  40. [46]Mandal S. Mallick N. Microalga Scenedesmus obliquus as a potential source for biodiesel production Applied Microbiology and Biotechnology 2009 84 2 281 291 10.1007/s00253-009-1935-6 2-s2.0-68749089610 19330327 · DOI
  41. [47]Sato A. Matsumura R. Hoshino N. Tsuzuki M. Sato N. Responsibility of regulatory gene expression and repressed protein synthesis for triacylglycerol accumulation on sulfur-starvation in Chlamydomonas reinhardtii Frontiers in Plant Science 2014 5, article 444 10.3389/fpls.2014.00444 2-s2.0-84908191789 PMC4160968 25309550 · DOI
  42. [48]Fernandes B. Teixeira J. Dragone G. Relationship between starch and lipid accumulation induced by nutrient depletion and replenishment in the microalga Parachlorella kessleri Bioresource Technology 2013 144 268 274 10.1016/j.biortech.2013.06.096 2-s2.0-84880675674 23876655 · DOI
  43. [49]Přibyl P. Cepák V. Zachleder V. Production of lipids in 10 strains of Chlorella and Parachlorella, and enhanced lipid productivity in Chlorella vulgaris Applied Microbiology and Biotechnology 2012 94 2 549 561 10.1007/s00253-012-3915-5 2-s2.0-84862646145 22361856 · DOI
  44. [50]Richmond A. Richmond A. Cell response to environmental factors CRC Handbook of Microalgal Mass Culture 1986 Florida, Fla, USA CRC Press 89 95
  45. [51]Alkayal F. Albion R. L. Tillett R. L. Hathwaik L. T. Lemos M. S. Cushman J. C. Expressed sequence tag (EST) profiling in hyper saline shocked Dunaliella salina reveals high expression of protein synthetic apparatus components Plant Science 2010 179 5 437 449 10.1016/j.plantsci.2010.07.001 2-s2.0-77956755250 21802602 · DOI
  46. [53]Yang H. He Q. Rong J. Xia L. Hu C. Rapid neutral lipid accumulation of the alkali-resistant oleaginous Monoraphidium dybowskii LB50 by NaCl induction Bioresource Technology 2014 172 131 137 10.1016/j.biortech.2014.08.066 2-s2.0-84907514879 25255189 · DOI
  47. [54]Kirrolia A. Bishnoia N. R. Singh N. Salinity as a factor affecting the physiological and biochemical traits of Scenedesmus quadricauda Journal of Algal Biomass Utilization 2011 2 28 34
  48. [55]Takagi M. Karseno Yoshida T. Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells Journal of Bioscience and Bioengineering 2006 101 3 223 226 10.1263/jbb.101.223 2-s2.0-33745727511 16716922 · DOI
  49. [56]Duan X. Ren G. Y. Liu L. L. Zhu W. X. Salt-induced osmotic stress for lipid overproduction in batch culture of Chlorella vulgaris African Journal Biotechnology 2012 11 27 7072 7078
  50. [57]Ren H.-Y. Liu B.-F. Kong F. Zhao L. Xie G.-J. Ren N.-Q. Enhanced lipid accumulation of green microalga Scenedesmus sp. by metal ions and EDTA addition Bioresource Technology 2014 169 763 767 10.1016/j.biortech.2014.06.062 2-s2.0-84907594946 25037828 · DOI
  51. [58]Yang J. Cao J. Xing G. Yuan H. Lipid production combined with biosorption and bioaccumulation of cadmium, copper, manganese and zinc by oleaginous microalgae Chlorella minutissima UTEX2341 Bioresource Technology 2015 175 537 544 10.1016/j.biortech.2014.10.124 2-s2.0-84910684825 25459865 · DOI
  52. [59]Liu Z.-Y. Wang G.-C. Zhou B.-C. Effect of iron on growth and lipid accumulation in Chlorella vulgaris Bioresource Technology 2008 99 11 4717 4722 10.1016/j.biortech.2007.09.073 2-s2.0-41849116000 17993270 · DOI
  53. [60]Li Y. Mu J. Chen D. Production of biomass and lipid by the microalgae Chlorella protothecoides with heterotrophic-Cu(II) stressed (HCuS) coupling cultivation Bioresource Technology 2013 148 283 292 10.1016/j.biortech.2013.08.153 2-s2.0-84884325496 24055971 · DOI
  54. [61]Mujtaba G. Choi W. Lee C.-G. Lee K. Lipid production by Chlorella vulgaris after a shift from nutrient-rich to nitrogen starvation conditions Bioresource Technology 2012 123 279 283 10.1016/j.biortech.2012.07.057 2-s2.0-84865539562 22940330 · DOI
  55. [62]Adams C. Godfrey V. Wahlen B. Seefeldt L. Bugbee B. Understanding precision nitrogen stress to optimize the growth and lipid content tradeoff in oleaginous green microalgae Bioresource Technology 2013 131 188 194 10.1016/j.biortech.2012.12.143 2-s2.0-84872702666 23347926 · DOI · Paper page
  56. [63]Zhao Y. Li D. Ding K. Production of biomass and lipids by the oleaginous microalgae Monoraphidium sp. QLY-1 through heterotrophic cultivation and photo-chemical modulator induction Bioresource Technology 2016 211 669 676 10.1016/j.biortech.2016.03.160 27058402 · DOI
  57. [64]Feng P. Deng Z. Fan L. Hu Z. Lipid accumulation and growth characteristics of Chlorella zofingiensis under different nitrate and phosphate concentrations Journal of Bioscience and Bioengineering 2012 114 4 405 410 10.1016/j.jbiosc.2012.05.007 2-s2.0-84865996900 22698727 · DOI · Paper page
  58. [65]Xin L. Hong-ying H. Jia Y. Lipid accumulation and nutrient removal properties of a newly isolated freshwater microalga, Scenedesmus sp. LX1, growing in secondary effluent New Biotechnology 2010 27 1 59 63 10.1016/j.nbt.2009.11.006 2-s2.0-77951787204 19969113 · DOI · Paper page
  59. [66]Álvarez-Díaz P. D. Ruiz J. Arbib Z. Barragán J. Garrido-Pérez C. Perales J. A. Lipid production of microalga Ankistrodesmus falcatus increased by nutrient and light starvation in a two-stage cultivation process Applied Biochemistry and Biotechnology 2014 174 4 1471 1483 10.1007/s12010-014-1126-5 2-s2.0-84920253481 25119548 · DOI
  60. [67]Ota S. Oshima K. Yamazaki T. Highly efficient lipid production in the green alga Parachlorella kessleri: draft genome and transcriptome endorsed by whole-cell 3D ultrastructure Biotechnology for Biofuels 2016 9, article 13 10.1186/s13068-016-0424-2 PMC4724957 26811738 · DOI
  61. [68]Mizuno Y. Sato A. Watanabe K. Sequential accumulation of starch and lipid induced by sulfur deficiency in Chlorella and Parachlorella species Bioresource Technology 2013 129 150 155 10.1016/j.biortech.2012.11.030 2-s2.0-84870943736 23238344 · DOI

Authors
Zhu, L. D., Li, Z. H., & Hiltunen, E.
Affiliations
  • Hubei University (CN)
  • University of Vaasa (FI)
Corresponding author
Zhu, L. D.
Venue
BioMed Research International
Publisher
Wiley
Published
2016
Volume
2016
Pages
1-8
ISSN
  • 1110-7243 (ISSN-L)
  • 2314-6133
  • 2314-6141
OpenAlex
W2522973931
Cited by
245
References
65
Citations by year
2026: 8 · 2025: 10 · 2024: 26 · 2023: 20 · 2022: 36 · 2021: 42 · 2020: 45 · 2019: 33 · 2018: 13 · 2017: 11 · 2016: 1
FWCI
0.71
Type
journal article
Language
en
Open access
Locations
  • BioMed Research International (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Osuva (University of Vaasa) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Kone Foundation in Finland
  • Botnia-Atlantica programme and European Regional Development Fund
Topics
  • Physical Sciences › Energy › Renewable Energy, Sustainability and the Environment › Algal biology and biofuel production
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Microbial Metabolic Engineering and Bioproduction
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
Keywords
microalgae, microalgal lipid accumulation, biodiesel feedstock, nutrient deprivation, nitrogen limitation, phosphorus limitation, sulfur limitation, light intensity, temperature effects, carbon dioxide, salt stress, metal stress, biofuels
MeSH terms
Biotechnology, Lipids, Stress, Physiological, Metabolic Networks and Pathways, Biofuels, Microalgae

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review