{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T10:54:55Z","timestamp":1790679295616,"version":"4.1.0"},"reference-count":45,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2020,5,23]],"date-time":"2020-05-23T00:00:00Z","timestamp":1590192000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"European Regional Development Fund of the European Union and Greek national funds","award":["call RESEARCH\u2013CREATE\u2013INNOVATE (project code: T1EDK-04223)"],"award-info":[{"award-number":["call RESEARCH\u2013CREATE\u2013INNOVATE (project code: T1EDK-04223)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>The effect of iron, manganese, phosphorus and nitrogen on growth and lipid synthesis of the microalgae Nannochloropsis oceanica CCMP1779, as well as their impact on the magnetic harvesting efficiency, are examined under their depriving cell culture conditions. Herein, it is demonstrated that nitrogen and manganese depletion primarily reduced cell growth while phosphorus and iron restriction led to higher dry biomass. Subsequently, the role of those nutrients on fatty acids profile was examined. Phosphorus and nitrogen restriction resulted in lower and higher lipid content, respectively. High amounts of polyunsaturated fatty acids like eicosapentaenoic acid are produced under iron and manganese depletion. Phosphorus deprivation favors monounsaturated fatty acids such as C18:1 and C16:1, while nitrogen restriction favors saturated fatty acid production like C14:0, C16:0 and C18:0. Since the presence\/absence of macro- and micro-elements may affect the overall electrostatic charges on the outmost microalgae surface, it was also analyzed how these elements affect the magnetic harvesting efficiency. Results showed that phosphorus deprivation led to the best magnetic harvesting efficiency of N. oceanica cells (93%) as compared to other nutrient starvation as well as standard medium.<\/jats:p>","DOI":"10.3390\/plants9050660","type":"journal-article","created":{"date-parts":[[2020,5,25]],"date-time":"2020-05-25T11:42:02Z","timestamp":1590406922000},"page":"660","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["A Study on the Effect of Macro- and Micro- Nutrients on Nannochloropsis oceanica Growth, Fatty Acid Composition and Magnetic Harvesting Efficiency"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8221-6865","authenticated-orcid":false,"given":"Maria G.","family":"Savvidou","sequence":"first","affiliation":[{"name":"Biotechnology Laboratory, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9942-4046","authenticated-orcid":false,"given":"Elenitsa","family":"Boli","sequence":"additional","affiliation":[{"name":"Laboratory of Thermodynamics and Transport Phenomena, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dimitrios","family":"Logothetis","sequence":"additional","affiliation":[{"name":"Laboratory of Thermodynamics and Transport Phenomena, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Theopisti","family":"Lymperopoulou","sequence":"additional","affiliation":[{"name":"Environment and Quality of Life Center, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2044-7569","authenticated-orcid":false,"given":"Angelo","family":"Ferraro","sequence":"additional","affiliation":[{"name":"Biotechnology Laboratory, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4238-1991","authenticated-orcid":false,"given":"Vasiliki","family":"Louli","sequence":"additional","affiliation":[{"name":"Laboratory of Thermodynamics and Transport Phenomena, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5198-6533","authenticated-orcid":false,"given":"Diomi","family":"Mamma","sequence":"additional","affiliation":[{"name":"Biotechnology Laboratory, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dimitris","family":"Kekos","sequence":"additional","affiliation":[{"name":"Biotechnology Laboratory, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kostis","family":"Magoulas","sequence":"additional","affiliation":[{"name":"Laboratory of Thermodynamics and Transport Phenomena, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fragiskos N.","family":"Kolisis","sequence":"additional","affiliation":[{"name":"Biotechnology Laboratory, School of Chemical Engineering, National Technical University of Athens, 9 Iroon Polytechniou Str, Zografou Campus, 15780 Athens, Greece"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,5,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1111\/pre.12160","article-title":"The effect of physicochemical conditions and nutrient sources on maximizing the growth and lipid productivity of green microalgae","volume":"65","year":"2017","journal-title":"Phycol. Res."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1155\/2013\/671545","article-title":"The effects of trace elements on the lipid productivity and fatty acid composition of Nannochloropis oculata","volume":"2013","author":"Dou","year":"2013","journal-title":"J. Renew. Energy"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Schmidt, S.B., and Soren, H. (2019). The biochemical properties of manganese in plants. Plants, 8.","DOI":"10.3390\/plants8100381"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/S0005-2728(00)00219-X","article-title":"EPR\/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster","volume":"1503","author":"Peloquin","year":"2001","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1007\/s12257-016-0628-0","article-title":"Effects of iron sources on the growth and lipid\/carbohydrate production of marine microalga Dunaliella tertiolecta","volume":"22","author":"Rizwan","year":"2017","journal-title":"Biotechnol. Bioprocess. Eng."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1080\/0967026032000157156","article-title":"Distribution of intracellular nitrogen in marine microalgae: Calculation of new nitrogen-to-protein conversion factors","volume":"39","author":"Barbarino","year":"2004","journal-title":"Eur. J. Phycol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1002\/lite.201200197","article-title":"Microlagae as an alternative source of omega-3-long chain polyunsaturated fatty acids","volume":"24","author":"Ryckebosch","year":"2012","journal-title":"Lipid Technol."},{"key":"ref_8","first-page":"973","article-title":"Effect of the culture nutrients on the biomass and lipid productivities of microalgae Dunaliella tertiolecta","volume":"32","author":"Mata","year":"2013","journal-title":"Chem. Eng."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1649","DOI":"10.1016\/j.biortech.2010.09.062","article-title":"Effect of nutrients on growth and lipid accumulation in the green algae Dunaliella tertiolecta","volume":"102","author":"Chen","year":"2011","journal-title":"Bioresour. Technol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1007\/s13213-014-0846-7","article-title":"Effect of Mn2+, Co2+ and H2O2 on biomass and lipids of the green microalga Chlorella vulgaris as a potential candidate for biodiesel production","volume":"65","author":"Battah","year":"2014","journal-title":"Ann. Microbiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1104\/pp.19.00854","article-title":"The Microalga Nannochloropsis during transition from quiescence to autotrophy in response to nitrogen availability","volume":"182","author":"Zienkiewicz","year":"2020","journal-title":"Plant. Physiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1111\/j.1529-8817.2007.00375.x","article-title":"Effect of nitrogen starvation on optical properties, pigments, and arachidonic acid content of the unicellular green alga Parietochlorisincisa (Trebouxiophyceae, Chlorophyta)","volume":"43","author":"Merzlyak","year":"2007","journal-title":"J. Phycol."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Satpati, G.G., Gorain, P.C., and PaL, R. (2016). Efficacy of EDTA and phosphorous on biomass yield and total lipid accumulation in two green microalgae with special emphasis on neutral lipid detection by flow cytometry. Adv. Biol.","DOI":"10.1155\/2016\/8712470"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1016\/j.biortech.2012.12.060","article-title":"Harvesting microalgae with microwave synthesized magnetic microparticles","volume":"130","author":"Prochazkova","year":"2013","journal-title":"Bioresour. Technol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1016\/j.jenvman.2018.03.019","article-title":"In-situ self-assembly of plant polyphenol-coated Fe3O4 particles for oleaginous microalgae harvesting","volume":"214","author":"Wang","year":"2018","journal-title":"J. Environ. Manag."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"11677","DOI":"10.1021\/acsami.5b03472","article-title":"Recovering magnetic Fe3O4\u2013ZnO nanocomposites from algal biomass based on hydrophobicity shift under UV irradiation","volume":"7","author":"Ge","year":"2015","journal-title":"ACS Appl. Mater. Interfaces"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Fraga-Garc\u00eda, P., Kubbutat, P., Brammen, M., Schwaminger, S., and Berensmeier, S. (2018). Bare Iron Oxide Nanoparticles for Magnetic Harvesting of Microalgae: From Interaction Behavior to Process Realization. Nanomaterials, 8.","DOI":"10.3390\/nano8050292"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"387","DOI":"10.1016\/j.biortech.2013.04.016","article-title":"Efficient harvesting of marine microalgae Nannochloropsis maritima using magnetic nanoparticles","volume":"138","author":"Hu","year":"2013","journal-title":"Bioresour. Technol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Boli, E., Savvidou, M., Logothetis, D., Louli, V., Pappa, G., Voutsas, E., and Magoulas, K. (2017). Magnetic harvesting of marine algae Nannochloropsis oceanica. Sep. Sci. Technol., 1\u20138.","DOI":"10.1080\/01496395.2017.1296463"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1016\/j.bcab.2017.04.006","article-title":"A study on the combined effects of carbon and nitrogen source on high added value products synthesis by Nannochloropsis oceanica CCMP1779 using response surface methodology","volume":"10","author":"Savvidou","year":"2017","journal-title":"Biocatal. Agric. Biotechnol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.enzmictec.2018.05.011","article-title":"Studies on the catalytic behavior of a membrane-bound lipolytic enzyme from the microalgae Nannochloropsis oceanica CCMP1779","volume":"116","author":"Savvidou","year":"2018","journal-title":"Enzym. Microb. Technol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1007\/s12010-014-1126-5","article-title":"Lipid production of microalga Ankistrodes musfalcatus increased by nutrient and light starvation in a two-stage cultivation process","volume":"174","author":"Ruiz","year":"2014","journal-title":"Appl. Biochem. Biotechnol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"785","DOI":"10.1093\/plankt\/8.4.785","article-title":"Effects of light and nitrogen limitation on the cell cycle of the dinoflagellate Amphidinium carteri","volume":"8","author":"Olson","year":"1986","journal-title":"J. Plankton Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1083\/jcb.131.4.1025","article-title":"Manganese effectively supports yeast cell-cycle progression in place of calcium","volume":"131","author":"Loukin","year":"1995","journal-title":"J. Cell Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"5763","DOI":"10.1093\/jxb\/ers225","article-title":"A typical iron storage in marine brown algae: A multidisciplinary study of iron transport and storage in Ectocarpus siliculosus","volume":"63","author":"Miller","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1016\/j.biortech.2013.12.109","article-title":"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","volume":"155","author":"Sun","year":"2014","journal-title":"Bioresour. Technol."},{"key":"ref_27","first-page":"295","article-title":"Phosphate-induced changes in fatty acid biosynthesis in Chlorella sp. KS-MA2 strain","volume":"97","author":"Ahmad","year":"2016","journal-title":"J. Biotechnol. Comput. Biol. Bionanotechnol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1007\/s10811-012-9865-6","article-title":"Effect of phosphorus on lipid accumulation in freshwater microalga Chlorella sp.","volume":"25","author":"Liang","year":"2013","journal-title":"J. Appl. Phycol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1856","DOI":"10.1128\/EC.00272-09","article-title":"Algal lipid bodies: Stress induction, purification, and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii","volume":"8","author":"Wang","year":"2009","journal-title":"Eukaryot. Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1146","DOI":"10.1016\/j.cep.2009.03.006","article-title":"Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production","volume":"48","author":"Converti","year":"2009","journal-title":"Chem. Eng. Process. Process. Intensif."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"6797","DOI":"10.1016\/j.biortech.2010.03.120","article-title":"Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions","volume":"101","author":"Lv","year":"2010","journal-title":"Bioresour. Technol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"4607","DOI":"10.3390\/en6094607","article-title":"Effects of environmental factors and nutrient availability on the biochemical composition of algae for biofuels production: A review","volume":"6","author":"Juneja","year":"2013","journal-title":"Energies"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1093\/jxb\/ers339","article-title":"Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana","volume":"64","author":"Millaleo","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1007\/s00284-006-0470-2","article-title":"Effects of iron on growth, pigment content, photosystem II efficiency, and siderophores production of Microcystis aeruginosa and Microcystis wesenbergii","volume":"55","author":"Xing","year":"2007","journal-title":"Curr. Microbiol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"10305","DOI":"10.1074\/jbc.M511057200","article-title":"A chlorophyll a\/b- binding protein homolog that is induced by iron deficiency is associated with enlarged photosystem I units in the eukaryotic alga Dunaliella Salina","volume":"281","author":"Varsano","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.ejar.2013.12.007","article-title":"Growth and fatty acid profile of the marine microalga Picochlorum sp. grown under nutrient stress conditions","volume":"39","year":"2013","journal-title":"Egypt. J. Aquat. Res."},{"key":"ref_37","first-page":"190","article-title":"Effect of nitrogen concentration on growth, lipid production and fatty acid profiles of the marine diatom Phaeodactylum tricornutum","volume":"51","author":"Yodsuwan","year":"2017","journal-title":"Agric. Nat. Resour."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1007\/s00248-017-0983-1","article-title":"Common and species-specific effects of phosphate on marine microalgae fatty acids shape their function in phytoplankton trophic ecology","volume":"74","author":"Armada","year":"2017","journal-title":"Microb. Ecol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"30246","DOI":"10.1074\/jbc.M113.490425","article-title":"Remodeling of membrane lipids in iron starved Chlamydomonas","volume":"288","author":"Urzica","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref_40","first-page":"19","article-title":"Growth, lipid content, and lipid profile of the green alga, Chlorella vulgaris Beij., under different concentrations of Fe and CO2","volume":"6","author":"Carpio","year":"2015","journal-title":"J. Eng. Sci. Technol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1016\/j.algal.2015.03.005","article-title":"Harvesting microalgae by magnetic separation: A review","volume":"9","author":"Wang","year":"2015","journal-title":"Algal Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1139\/m62-029","article-title":"Studies of Marine Planktonic Diatoms: I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran","volume":"8","author":"Guillard","year":"1962","journal-title":"Can. J. Microbiol."},{"key":"ref_43","first-page":"586","article-title":"Extraction and quantification of pigments from a marine microalga: A simple and reproducible method","volume":"2","author":"Henriques","year":"2007","journal-title":"Commun. Curr. Res. Educ. Top. Trends Appl. Microbiol. Formatex"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1623","DOI":"10.1007\/s10811-012-9825-1","article-title":"Effects of initial population density (IPD) on growth and lipid composition of Nannochloropsis sp.","volume":"24","author":"Chen","year":"2012","journal-title":"J. Appl. Phycol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"934","DOI":"10.1093\/chromsci\/bms093","article-title":"Determination of Free Fatty Acids and Triglycerides by gas Chromatography Using Selective Esterification Reactions","volume":"50","author":"Kail","year":"2012","journal-title":"J. Chromatogr. Sci."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/9\/5\/660\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:31:43Z","timestamp":1760175103000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/9\/5\/660"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,23]]},"references-count":45,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2020,5]]}},"alternative-id":["plants9050660"],"URL":"https:\/\/doi.org\/10.3390\/plants9050660","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,5,23]]}}}