Microalgae as Sustainable Biofactories to Produce High-Value Lipids: Biodiversity, Exploitation, and Biotechnological Applications

Microalgae are often called “sustainable biofactories” due to their dual potential to mitigate atmospheric carbon dioxide and produce a great diversity of high-value compounds. Nevertheless, the successful exploitation of microalgae as biofactories for industrial scale is dependent on choosing the right microalga and optimum growth conditions. Due to the rich biodiversity of microalgae, a screening pipeline should be developed to perform microalgal strain selection exploring their growth, robustness, and metabolite production. Current prospects in microalgal biotechnology are turning their focus to high-value lipids for pharmaceutic, nutraceutic, and cosmetic products. Within microalgal lipid fraction, polyunsaturated fatty acids and carotenoids are broadly recognized for their vital functions in human organisms. Microalgal-derived phytosterols are still an underexploited lipid resource despite presenting promising biological activities, including neuroprotective, anti-inflammatory, anti-cancer, neuromodulatory, immunomodulatory, and apoptosis inductive effects. To modulate microalgal biochemical composition, according to the intended field of application, it is important to know the contribution of each cultivation factor, or their combined effects, for the wanted product accumulation. Microalgae have a vital role to play in future low-carbon economy. Since microalgal biodiesel is still costly, it is desirable to explore the potential of oleaginous species for its high-value lipids which present great global market prospects.

[1]  F. Mahmud,et al.  Microalgae biofuels production: A systematic review on socioeconomic prospects of microalgae biofuels and policy implications , 2021 .

[2]  M. Mofijur,et al.  Strategies to Produce Cost-Effective Third-Generation Biofuel From Microalgae , 2021, Frontiers in Energy Research.

[3]  Yongteng Zhao,et al.  A fed-batch feeding with succinic acid strategy for astaxanthin and lipid hyper-production in Haematococcus pluviualis. , 2021, Bioresource technology.

[4]  S. Sim,et al.  Robust cyst germination induction in Haematococcus pluvialis to enhance astaxanthin productivity in a semi-continuous outdoor culture system using power plant flue gas. , 2021, Bioresource technology.

[5]  E. Ibáñez,et al.  Phytosterol-rich compressed fluids extracts from Phormidium autumnale cyanobacteria with neuroprotective potential , 2021 .

[6]  R. Wagner,et al.  Sterols Biosynthesis in Algae , 2021, Biosynthesis [Working Title].

[7]  Xingyu Li,et al.  Simultaneous improvement of astaxanthin and lipid production of Haematococcus pluvialis by using walnut shell extracts , 2021 .

[8]  E. Filaire,et al.  Microalgae n-3 PUFAs Production and Use in Food and Feed Industries , 2021, Marine drugs.

[9]  D. F. Basri,et al.  In Vitro and in Vivo Cytotoxic Effects of Chlorella Against Various types of Cancer , 2021 .

[10]  Shoyeb Khan,et al.  Treatment of Wastewaters by Microalgae and the Potential Applications of the Produced Biomass—A Review , 2020, Water.

[11]  Y. Jeon,et al.  In vitro and in vivo anti-inflammatory activities of a sterol-enriched fraction from freshwater green alga, Spirogyra sp. , 2020 .

[12]  A. Baby,et al.  (Bio)Technological aspects of microalgae pigments for cosmetics , 2020, Applied Microbiology and Biotechnology.

[13]  Xupeng Cao,et al.  A Quick Look Back at the Microalgal Biofuel Patents: Rise and Fall , 2020, Frontiers in Bioengineering and Biotechnology.

[14]  C. Rad-Menéndez,et al.  Patent depositing of algal strains , 2020, Applied Phycology.

[15]  S. Sukhikh,et al.  Microalgae: A Promising Source of Valuable Bioproducts , 2020, Biomolecules.

[16]  Marina L Díaz,et al.  Crosstalk between sterol and neutral lipid metabolism in the alga Haematococcus pluvialis exposed to light stress. , 2020, Biochimica et biophysica acta. Molecular and cell biology of lipids.

[17]  H. Yoon,et al.  Nitrogen Deficiency-Dependent Abiotic Stress Enhances Carotenoid Production in Indigenous Green Microalga Scenedesmus rubescens KNUA042, for Use as a Potential Resource of High Value Products , 2020 .

[18]  M. Tabarzad,et al.  Anti-inflammatory Activity of Bioactive Compounds from Microalgae and Cyanobacteria by Focusing on the Mechanisms of Action , 2020, Molecular Biology Reports.

[19]  C. Theodoropoulos,et al.  Microalgae strain catalogue: a strain selection guide for microalgae users: cultivation and chemical characteristics for high added-value products (2nd Edition) , 2020 .

[20]  M. Dudek,et al.  The Cultivation of Lipid-Rich Microalgae Biomass as Anaerobic Digestate Valorization Technology—A Pilot-Scale Study , 2020 .

[21]  P. Ralph,et al.  Levels of Diatom Minor Sterols Respond to Changes in Temperature and Salinity , 2020, Journal of Marine Science and Engineering.

[22]  A. Martel,et al.  Exploring Pavlova pinguis chemical diversity: a potentially novel source of high value compounds , 2020, Scientific Reports.

[23]  D. Lagadic-Gossmann,et al.  Microalgal carotenoids and phytosterols regulate biochemical mechanisms involved in human health and disease prevention. , 2019, Biochimie.

[24]  S. Mudliar,et al.  Recent Advances in Microalgal Bioactives for Food, Feed, and Healthcare Products: Commercial Potential, Market Space, and Sustainability. , 2019, Comprehensive reviews in food science and food safety.

[25]  J. Harwood Algae: Critical Sources of Very Long-Chain Polyunsaturated Fatty Acids , 2019, Biomolecules.

[26]  Meng Chen,et al.  Stoichiometric and sterol responses of dinoflagellates to changes in temperature, nutrient supply and growth phase , 2019, Algal Research.

[27]  Liangxiao Zhang,et al.  Phytosterol Contents of Edible Oils and Their Contributions to Estimated Phytosterol Intake in the Chinese Diet , 2019, Foods.

[28]  Gokare A. Ravishankar,et al.  Global Microalgal-Based Products for Industrial Applications , 2019, Handbook of Algal Technologies and Phytochemicals.

[29]  Wei-hong Jin,et al.  Effect of organic carbon to nitrogen ratio in wastewater on growth, nutrient uptake and lipid accumulation of a mixotrophic microalgae Chlorella sp. , 2019, Bioresource technology.

[30]  C. González-López,et al.  NMR Metabolomics as an Effective Tool To Unravel the Effect of Light Intensity and Temperature on the Composition of the Marine Microalgae Isochrysis galbana. , 2019, Journal of agricultural and food chemistry.

[31]  A. Marzocchella,et al.  Current Bottlenecks and Challenges of the Microalgal Biorefinery. , 2019, Trends in biotechnology.

[32]  M. Francavilla,et al.  Extracts from Microalga Chlorella sorokiniana Exert an Anti-Proliferative Effect and Modulate Cytokines in Sheep Peripheral Blood Mononuclear Cells , 2019, Animals : an open access journal from MDPI.

[33]  Y. Keum,et al.  Microbial platforms to produce commercially vital carotenoids at industrial scale: an updated review of critical issues , 2019, Journal of Industrial Microbiology & Biotechnology.

[34]  V. Piironen,et al.  Integrated utilization of microalgae cultured in aquaculture wastewater: wastewater treatment and production of valuable fatty acids and tocopherols , 2018, Journal of Applied Phycology.

[35]  S. Vaidyanathan,et al.  The Effect of High-Intensity Ultraviolet Light to Elicit Microalgal Cell Lysis and Enhance Lipid Extraction , 2018, Metabolites.

[36]  K. Poluri,et al.  Leveraging algal omics to reveal potential targets for augmenting TAG accumulation. , 2018, Biotechnology advances.

[37]  Changfu Zhu,et al.  A global perspective on carotenoids: Metabolism, biotechnology, and benefits for nutrition and health. , 2018, Progress in lipid research.

[38]  Jiangxin Wang,et al.  Growth and lipid accumulation by different nutrients in the microalga Chlamydomonas reinhardtii , 2018, Biotechnology for Biofuels.

[39]  M. Borowitzka Biology of microalgae , 2018 .

[40]  A. Ramli,et al.  A Review on Methods Used in Analysis of Microalgae Lipid Composition , 2017 .

[41]  H. Elissen,et al.  Socio-economic assessment of Algae-based PUFA production , 2017 .

[42]  T. Juhna,et al.  Review on Challenges and Limitations for Algae-Based Wastewater Treatment , 2017 .

[43]  Eliseu Rodrigues,et al.  Effect of temperature and nitrogen concentration on biomass composition of Heterochlorella luteoviridis , 2017 .

[44]  J. Cadoret,et al.  Effects of growth phase and nitrogen limitation on biochemical composition of two strains of Tisochrysis lutea , 2017 .

[45]  M. Borowitzka,et al.  Scaling up microalgal cultures to commercial scale , 2017 .

[46]  H. Kleivdal,et al.  Bioprospecting North Atlantic microalgae with fast growth and high polyunsaturated fatty acid (PUFA) content for microalgae-based technologies , 2017, Algal research.

[47]  S. Viamajala,et al.  Cultivation of Microalgae at Extreme Alkaline pH Conditions: A Novel Approach for Biofuel Production , 2017 .

[48]  P. Schenk,et al.  UV-C radiation increases sterol production in the microalga Pavlova lutheri. , 2017, Phytochemistry.

[49]  R. Marino,et al.  Phytosterols from Dunaliella tertiolecta Reduce Cell Proliferation in Sheep Fed Flaxseed during Post Partum , 2017, Marine drugs.

[50]  N. Cordeiro,et al.  Marine microalgae monosaccharide fluctuations as a stress response to nutrients inputs , 2017 .

[51]  J. Perales,et al.  Freshwater microalgae selection for simultaneous wastewater nutrient removal and lipid production , 2017 .

[52]  A. Solovchenko,et al.  Effects of CO2 enrichment on primary photochemistry, growth and astaxanthin accumulation in the chlorophyte Haematococcus pluvialis. , 2017, Journal of photochemistry and photobiology. B, Biology.

[53]  M. K. Mandal,et al.  Production of biodiesel from microalgae through biological carbon capture: a review , 2017, 3 Biotech.

[54]  M. M. Barrado-Moreno,et al.  Degradation of microalgae from freshwater by UV radiation , 2017 .

[55]  M. Santana-Casiano,et al.  Production of Primary and Secondary Metabolites Using Algae , 2017 .

[56]  Y. Jeon,et al.  Anti-inflammatory and anti-cancer activities of sterol rich fraction of cultured marine microalga Nannochloropsis oculata , 2016 .

[57]  N. Cordeiro,et al.  Changes in fatty acid biosynthesis in marine microalgae as a response to medium nutrient availability , 2016 .

[58]  Georgios Panis,et al.  Commercial astaxanthin production derived by green alga Haematococcus pluvialis: A microalgae process model and a techno-economic assessment all through production line , 2016 .

[59]  N. Cordeiro,et al.  Marine microalgae growth and carbon partitioning as a function of nutrient availability. , 2016, Bioresource technology.

[60]  Tianzhong Liu,et al.  Concurrent production of carotenoids and lipid by a filamentous microalga Trentepohlia arborum. , 2016, Bioresource technology.

[61]  C. Barrow,et al.  A Review on the Assessment of Stress Conditions for Simultaneous Production of Microalgal Lipids and Carotenoids , 2016, Front. Microbiol..

[62]  M. Domingues,et al.  Lipidomic Approaches towards Deciphering Glycolipids from Microalgae as a Reservoir of Bioactive Lipids , 2016, Marine drugs.

[63]  Jay J. Cheng,et al.  Astaxanthin-Producing Green Microalga Haematococcus pluvialis: From Single Cell to High Value Commercial Products , 2016, Front. Plant Sci..

[64]  Poonam Singh,et al.  Trends and novel strategies for enhancing lipid accumulation and quality in microalgae , 2016 .

[65]  A. Simopoulos An Increase in the Omega-6/Omega-3 Fatty Acid Ratio Increases the Risk for Obesity , 2016, Nutrients.

[66]  I. Khozin‐Goldberg Lipid Metabolism in Microalgae , 2016 .

[67]  J. Volkman Sterols in Microalgae , 2016 .

[68]  M. Morançais,et al.  Proteins and Pigments , 2016 .

[69]  Sandhya Mishra,et al.  Selective carotenoid accumulation by varying nutrient media and salinity in Synechocystis sp. CCNM 2501. , 2015, Bioresource technology.

[70]  M. Melkonian,et al.  Continuous removal of zinc from wastewater and mine dump leachate by a microalgal biofilm PSBR. , 2015, Journal of hazardous materials.

[71]  Zhiyong Liu,et al.  Ethanol induced astaxanthin accumulation and transcriptional expression of carotenogenic genes in Haematococcus pluvialis. , 2015, Enzyme and microbial technology.

[72]  S. Rocha,et al.  Chlorophyta and Rhodophyta macroalgae: a source of health promoting phytochemicals. , 2015, Food chemistry.

[73]  Wenxu Zhou,et al.  Pavlova lutheri is a high-level producer of phytosterols , 2015 .

[74]  Wei Zhang,et al.  Advances in Microalgae-Derived Phytosterols for Functional Food and Pharmaceutical Applications , 2015, Marine drugs.

[75]  T. Jurczak,et al.  The multidisciplinary approach to safety and toxicity assessment of microalgae-based food supplements following clinical cases of poisoning , 2015 .

[76]  Sandhya Mishra,et al.  A euryhaline Nannochloropsis gaditana with potential for nutraceutical (EPA) and biodiesel production , 2015 .

[77]  Ragnar Tveterås,et al.  A techno-economic analysis of industrial production of marine microalgae as a source of EPA and DHA-rich raw material for aquafeed: Research challenges and possibilities , 2015 .

[78]  M. Arita,et al.  Role of omega-3 fatty acids and their metabolites in asthma and allergic diseases. , 2015, Allergology international : official journal of the Japanese Society of Allergology.

[79]  J. Spruijt,et al.  Inventory of North-West European algae initiatives , 2015 .

[80]  J. Tattersall,et al.  Chapter 1 – General Overview , 2015 .

[81]  Yalei Zhang,et al.  Strategic enhancement of algal biomass, nutrient uptake and lipid through statistical optimization of nutrient supplementation in coupling Scenedesmus obliquus-like microalgae cultivation and municipal wastewater treatment. , 2014, Bioresource technology.

[82]  Y. Gibon,et al.  Metabolite Profiling and Integrative Modeling Reveal Metabolic Constraints for Carbon Partitioning under Nitrogen Starvation in the Green Algae Haematococcus pluvialis* , 2014, The Journal of Biological Chemistry.

[83]  M. S. Omar-Fauzee,et al.  Anti-inflammatory and anti-pyretic properties of Spirulina platensis and Spirulina lonar: a comparative study. , 2014, Pakistan journal of pharmaceutical sciences.

[84]  Amanda C. Martin,et al.  Evaluating solvent extraction systems using metabolomics approaches , 2014 .

[85]  D. Gilroy,et al.  Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. , 2014, Immunity.

[86]  Xiaoli Chai,et al.  Characterization of microalgae-bacteria consortium cultured in landfill leachate for carbon fixation and lipid production. , 2014, Bioresource technology.

[87]  C. Brunet,et al.  The Challenge of Ecophysiological Biodiversity for Biotechnological Applications of Marine Microalgae , 2014, Marine drugs.

[88]  AiDong Sun,et al.  Analysis of Polyphenols in Apple Pomace using Gas Chromatography-Mass Spectrometry with Derivatization , 2014 .

[89]  F. Bux,et al.  Overview of the potential of microalgae for CO2 sequestration , 2014, International Journal of Environmental Science and Technology.

[90]  B. Palsson,et al.  Effects of abiotic stressors on lutein production in the green microalga Dunaliella salina , 2014, Microbial Cell Factories.

[91]  S. Claus,et al.  The European Marine Observation and Data Network (EMODnet) central portal , 2014 .

[92]  P. Winge,et al.  Pathways of Lipid Metabolism in Marine Algae, Co-Expression Network, Bottlenecks and Candidate Genes for Enhanced Production of EPA and DHA in Species of Chromista , 2013, Marine drugs.

[93]  Alane Beatriz Vermelho,et al.  Allelopathy as a potential strategy to improve microalgae cultivation , 2013, Biotechnology for Biofuels.

[94]  P. Andrade,et al.  Sterols in Algae and Health , 2013 .

[95]  K. Heimann,et al.  Salinity Tolerance of Picochlorum atomus and the Use of Salinity for Contamination Control by the Freshwater Cyanobacterium Pseudanabaena limnetica , 2013, PloS one.

[96]  Vishal Gupta,et al.  Central metabolic processes of marine macrophytic algae revealed from NMR based metabolome analysis , 2013 .

[97]  G. Torzillo,et al.  Photosynthesis in Microalgae , 2013 .

[98]  Q. Cui,et al.  Metabolic profiles of Nannochloropsis oceanica IMET1 under nitrogen-deficiency stress. , 2013, Bioresource technology.

[99]  Xuxiong Huang,et al.  Effects of nitrogen supplementation of the culture medium on the growth, total lipid content and fatty acid profiles of three microalgae (Tetraselmis subcordiformis, Nannochloropsis oculata and Pavlova viridis) , 2013, Journal of Applied Phycology.

[100]  René H Wijffels,et al.  Carotenoid and fatty acid metabolism in nitrogen-starved Dunaliella salina, a unicellular green microalga. , 2012, Journal of biotechnology.

[101]  M. Francavilla,et al.  A mixture of phytosterols from Dunaliella tertiolecta affects proliferation of peripheral blood mononuclear cells and cytokine production in sheep. , 2012, Veterinary immunology and immunopathology.

[102]  Mingchun Li,et al.  Identification of a novel C22-∆4-producing docosahexaenoic acid (DHA) specific polyunsaturated fatty acid desaturase gene from Isochrysis galbana and its expression in Saccharomyces cerevisiae , 2012, Biotechnology Letters.

[103]  M. Lohr,et al.  Microalgae in the postgenomic era: a blooming reservoir for new natural products. , 2012, FEMS microbiology reviews.

[104]  Peer M. Schenk,et al.  Microalgae Isolation and Selection for Prospective Biodiesel Production , 2012 .

[105]  V. Cuomo,et al.  Extraction, characterization and in vivo neuromodulatory activity of phytosterols from microalga Dunaliella tertiolecta. , 2012, Current medicinal chemistry.

[106]  A. Wacker,et al.  Phytoplankton sterol contents vary with temperature, phosphorus and silicate supply: a study on three freshwater species , 2012 .

[107]  P. Cheung,et al.  +UVA treatment increases the degree of unsaturation in microalgal fatty acids and total carotenoid content in Nitzschia closterium (Bacillariophyceae) and Isochrysis zhangjiangensis (Chrysophyceae). , 2011, Food chemistry.

[108]  S. Harrison,et al.  Advantages and Challenges of Microalgae as a Source of Oil for Biodiesel , 2011 .

[109]  Shengjun Luo,et al.  Biomass and lipid production of marine microalgae using municipal wastewater and high concentration of CO2 , 2011 .

[110]  Z. Cohen,et al.  LC-PUFA from photosynthetic microalgae: occurrence, biosynthesis, and prospects in biotechnology , 2011, Applied Microbiology and Biotechnology.

[111]  Jianfeng Xu,et al.  Ettlia oleoabundans growth and oil production on agricultural anaerobic waste effluents. , 2011, Bioresource technology.

[112]  A. Wacker,et al.  Simultaneous Effects of Light Intensity and Phosphorus Supply on the Sterol Content of Phytoplankton , 2010, PloS one.

[113]  C. Kemfert,et al.  An overview of biofuel policies across the world , 2010 .

[114]  Raymond Turner,et al.  Insights on Innovation , 2010 .

[115]  R. Luque,et al.  Phytosterols from Dunaliella tertiolecta and Dunaliella salina: a potentially novel industrial application. , 2010, Bioresource technology.

[116]  E. Nelson,et al.  Effects of long-chain polyunsaturated fatty acid supplementation on neurodevelopment in childhood: a review of human studies. , 2010, Prostaglandins, leukotrienes, and essential fatty acids.

[117]  Xihui Zhang,et al.  The effects of sub-lethal UV-C irradiation on growth and cell integrity of cyanobacteria and green algae. , 2010, Chemosphere.

[118]  G. Nicholson,et al.  Determination of astaxanthin and astaxanthin esters in the microalgae Haematococcus pluvialis by LC-(APCI)MS and characterization of predominant carotenoid isomers by NMR spectroscopy , 2009, Analytical and bioanalytical chemistry.

[119]  D. Bilanović,et al.  Freshwater and marine microalgae sequestering of CO2 at different C and N concentrations – Response surface methodology analysis , 2009 .

[120]  Z. Cohen,et al.  Microbial and algal oils: Do they have a future for biodiesel or as commodity oils? , 2008 .

[121]  Ji-Young Lee,et al.  Lipid extract of Nostoc commune var. sphaeroides Kutzing, a blue-green alga, inhibits the activation of sterol regulatory element binding proteins in HepG2 cells. , 2008, The Journal of nutrition.

[122]  P. Fernandes,et al.  Phytosterols: applications and recovery methods. , 2007, Bioresource technology.

[123]  U. Das,et al.  Essential fatty acids: biochemistry, physiology and pathology , 2006, Biotechnology journal.

[124]  J. Beardall,et al.  Effects of nitrogen source and UV radiation on the growth, chlorophyll fluorescence and fatty acid composition of Phaeodactylum tricornutum and Chaetoceros muelleri (Bacillariophyceae). , 2006, Journal of photochemistry and photobiology. B, Biology.

[125]  F. Xavier Malcata,et al.  Optimization of ω-3 fatty acid production by microalgae: crossover effects of CO2 and light intensity under batch and continuous cultivation modes , 2005, Marine Biotechnology.

[126]  O. Pulz,et al.  Valuable products from biotechnology of microalgae , 2004, Applied Microbiology and Biotechnology.

[127]  M Fini,et al.  In vitro and in vivo tests for the biological evaluation of candidate orthopedic materials: Benefits and limits. , 2003, Journal of applied biomaterials & biomechanics : JABB.

[128]  K. B. Hicks,et al.  Phytosterols, phytostanols, and their conjugates in foods: structural diversity, quantitative analysis, and health-promoting uses. , 2002, Progress in lipid research.

[129]  S. Rawsthorne Carbon flux and fatty acid synthesis in plants. , 2002, Progress in lipid research.

[130]  M. Raeini-Sarjaz,et al.  Cholesterol-lowering efficacy of a sitostanol-containing phytosterol mixture with a prudent diet in hyperlipidemic men. , 1999, The American journal of clinical nutrition.

[131]  A. Sukenik,et al.  Effects of nitrogen source and growth phase on proximate biochemical composition, lipid classes and fatty acid profile of the marine microalga Isochrysis galbana , 1998 .

[132]  H. Kumar,et al.  Chlorophyta , 1992, Seaweeds of the Southeastern United States.

[133]  A. Sukenik Ecophysiological considerations in the optimization of eicosapentaenoic acid production by Nannochloropsis sp. (Eustigmatophyceae) , 1991 .