Abstract
This study aimed to investigate fatty acid content and productivity of the insufficiently investigated group of freshwater microalgae—desmids (Zygnematophyceae, Streptophyta)—and to estimate their commercial potential. A total of 29 desmid strains of various environmental preferences were grown in standard cultivation conditions to assess fatty acid concentration and composition and biomass productivity during the growth phases. Six desmid strains belonging to Cosmarium crenatum var. boldtianum, C. meneghinii, C. regnellii var. pseudoregnellii, C. leave, Staurastrum boreale, and S. punctulatum had distinctly high total fatty acid contents (> 200 mg g−1 dry weight), among which C. crenatum had by far the highest average of total fatty acids (308.1 mg g−1 dry weight). Despite that desmids were grown in a medium which was not enriched with nutrients and CO2, these six strains achieved moderate biomass productivity (up to 0.14 g dry weight L−1 day−1), while the fatty acid productivity was in the range 8–11.1 mg L−1 day−1. The relatively high amounts of linoleic and palmitic acids in C. crenatum var. boldtianum and C. meneghinii were comparable to those found in several commercially grown plants, indicating that fatty acid extracts of these desmids could be utilized in cosmetics, pharmacy, medicine, or in additional industrial applications. On the other hand, the high proportion of oleic acid in a new isolate of Staurastrum boreale, along with its relatively high biomass productivity and cell size, pointed that this strain might be used for further investigations regarding biodiesel production.
Similar content being viewed by others
References
Abomohra AEF, Wagner M, El-Sheekh M, Hanelt D (2013) Lipid and total fatty acid productivity in photoautotrophic fresh water microalgae: screening studies towards biodiesel production. J Appl Phycol 25:931–936
Abomohra AEF, Jin W, Tu R, Han S-F, Eid M, Eladel H (2016) Microalgal biomass production as a sustainable feedstock for biodiesel: current status and perspectives. Renew Sust Energ Rev 64:596–606
Abomohra AEF, El-Sheekh M, Hanelt D (2017) Screening of marine microalgae isolated from the hypersaline Bardawil lagoon for biodiesel feedstock. Renew Energ 101:1266–1272
Abomohra AEF, Eladel H, El-Esawi M, Wang S, Wang Q, He Z, Feng Y, Shang H, Hanelt D (2018) Effect of lipid-free microalgal biomass and waste glycerol on growth and lipid production of Scenedesmus obliquus: innovative waste recycling for extraordinary lipid production. Bioresour Technol 249:992–999
Aminul Islam M, Magnusson M, Brown RJ, Ayoko GA, Nabi MN, Heimann K (2013) Microalgal species selection for biodiesel production based on fuel properties derived from fatty acid profiles. Energies 6:5676–5702
Ando H, Ryu A, Hashimoto A, Oka M, Ichihashi M (1998) Linoleic acid and α-linolenic acid lightens ultraviolet-induced hyperpigmentation of the skin. Arch Dermatol Res 290:375–381
ASTM D6751-08 International (2008) Standard specification for biodiesel fuel blend stock (B100) for middle distillate fuels. ASTM D6751-08, ASTM International, West Conshohocken
Barabás I, Todoruţ IA (2011) Biodiesel quality, standards and properties. In: Montero G (ed) Biodiesel-quality, emissions and by-products. InTech Open, Rijeka, pp 3–28
Beudeker RF, Tabita FR (1983) Control of photorespiration glycolate metabolism in an oxygen-resistant mutant of Chlorella sorokiniana. J Bacteriol 155:650–656
Borowitzka MA (2013a) Energy from microalgae: a short history. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 1–5
Borowitzka M (2013b) Species and strain selection. In: Moheimani NR (ed) Borowitzka MA. Algae for biofuels and energy. Springer, Dordrecht, pp 77–89
Brook AJ (1981) The biology of desmids. Blackwell Scientific Publications, Oxford
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306
Coesel PFM (1991) Ammonium dependency in Closterium aciculare T. West, a planktonic desmid from alkaline, eutrophic waters. J Plankton Res 13:913–922
Coesel PFM, Meesters KJ (2007) Desmids of the lowlands. KNNV Publishing, Zeist
Collyer DM, Fogg GE (1954) Studies on fat accumulation by algae. J Exp Bot 6:256–275
Darmstadt GL, Mao-Qiang M, Chi E, Saha SK, Ziboh VA, Black RE, Santosham M, Elias PM (2002) Impact of topical oils on the skin barrier: possible implications for neonatal health in developing countries. Acta Paediatr 91:546–554
Dayananda C, Sarada R, Ushua RM, Shamala TR, Ravishankar GA (2007) Autotrophic cultivation of Botryococcus braunii for the production of hydrocarbons and exopolysaccharides in various media. Biomass Bioenergy 31:87–93
de Jaeger L, Verbeek REM, 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 7:69
de la Peña MR (2007) Cell growth and nutritive value of the tropical benthic diatom, Amphora sp., at varying levels of nutrients and light intensity, and different culture locations. J Appl Phycol 19:647–655
Demirbas MF (2011) Biofuels from algae for sustainable development. Appl Energ 88:3473–3480
Doan TTY, Sivaloganathan B, Obbard JP (2011) Screening of marine microalgae for biodiesel feedstock. Biomass Bioenergy 35:2534–2544
Draaisma RB, Wijffels RH, Slegers PM, Brentner LB, Roy A, Barbosa MJ (2013) Food commodities from microalgae. Curr Opin Biotechnol 24:169–177
El-Sheekh M, Abomohra AEF (2016) Biodiesel production from microalgae. In: Garg N, Aeron A (eds) Industrial microbiology: microbes in action. Nova Science Publishers, New York, pp 1–13
El-Sheekh MM, El-Gamal A, Bastawess AE, El-Bokhomy A (2017) Production and characterization of biodiesel from the unicellular green alga Scenedesmus obliquus, Energy Sources A 39:783–792
EN 14214 European Committee for Standardization (2008) Automotive fuels – fatty acid methylesters (fame) for diesel engines – requirements and test methods. EN14214, European Committee for Standardization
Francisco ÉC, Neves DB, Jacob-Lopes E, Franco TT (2010) Microalgae as feedstock for biodiesel production: carbon dioxide sequestration, lipid production and biofuel quality. J Chem Technol Biotechnol 85:395–403
Fužinato S, Cvijan M, Stamenković M (2011a) A checklist of desmids (Conjugatophyceae, Chlorophyta) of Serbia. II. Genus Cosmarium. Cryptogamie Algol 32:77–95
Fužinato S, Cvijan M, Krizmanić J (2011b) A checklist of desmids (Conjugatophyceae, Chlorophyta) of Serbia. III. Genus Staurastrum. Cryptogamie Algol 32:363–377
Goncalves EC, Johnson JV, Rathinasabapathi B (2013) Conversion of membrane lipid acyl groups to triacylglycerol and formation of lipid bodies upon nitrogen starvation in biofuel green algae Chlorella UTEX29. Planta 238:895–906
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 14:1649–1660
Greenspan P, Mayer EP, Fowler SD (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100:965–973
Griffiths MJ, Harrison ST (2009) Lipid productivity as a key characteristic for choosing algal species for biodiesel production. J Appl Phycol 21:493–507
Griffiths MJ, van Hille RP, Harrison STL (2012) Lipid productivity, settling potential and fatty acid profile of 11 microalgal species grown under nitrogen replete and limited conditions. J Appl Phycol 24:989–1001
Gunstone FD (2011) Vegetable oils in food technology – composition, properties and uses. Blackwell Publishing Ltd., Oxford
Harwood JL (1998) Fatty acid metabolism. Annu Rev Plant Physiol Plant Mol Biol 39:101–138
Hempel N, Petrick I, Behrendt F (2012) Biomass productivity and productivity of fatty acids and amino acids of microalgae strains as key characteristics of suitability for biodiesel production. J Appl Phycol 24:1407–1418
Henley WJ, Litaker WR, Novoveská L, Duke CS, Quemada HD, Sayre RT (2013) Initial risk assessment of genetically modified (GM) algae for commodity-scale cultivation. Algal Res 2:66–77
Hoekman SK, Broch A, Robbins C, Ceniceros E, Natarajan M (2012) Review of biodiesel composition, properties, and specifications. Renew Sust Energ Rev 16:143–169
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 54:621–639
Illman AM, Scragg AH, Shales SW (2000) Increase in Chlorella strains calorific values when grown in low nitrogen medium. Enzyme Microb Tech 27:631–635
Jones LA, King CC (1996) Cottonseed oil. In: Hui YH (ed) Bailey’s industrial oil and fat products, edible oil and fat products: oils and oilseeds. Wiley, New York, pp 159–240
Knothe GH (2005) Dependence of biodiesel fuel properties on the structure of fatty acid alkyl esters. Fuel Process Technol 86:1059–1070
Knothe GH (2011) A technical evaluation of biodiesel from vegetable oils vs. algae, will algae-derived biodiesel perform? Green Chem 13:3048–3065
Kokkinos N, Lazaridou A, Stamatis N, Orfanidis S, Mitropoulos AC, Christoforidis A, Nikolaou N (2015) Biodiesel production from selected microalgae strains and determination of its properties and combustion specific characteristics. J Engin Sci Techn Rev 8:1–6
Lang I, Hodac L, Friedl T, Feussner I (2011) Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection. BMC Plant Biol 11:124
Lapuerta M, Rodríguez-Fernández J, De Mora EF (2009) Correlation for the estimation of the cetane number of biodiesel fuels and implications on the iodine number. Energ Policy 37:4337–4344
Laurens LML (2017) State of technology review – algae bioenergy, an IEA bioenergy inter-task strategic project. National Renewable Energy Laboratory, Golden, Colorado
Lenzenweger R (1997) Desmidiaceenflora von Östereich, Teil 2, Bibliotheca Phycologica 102. Schweizerbart Science Publishers, Stuttgart
Lenzenweger R (1999) Desmidiaceenflora von Östereich, Teil 3, Bibliotheca Phycologica 104. Schweizerbart Science Publishers, Stuttgart
León-Saiki GM, Cabrero Martí T, van der Veen D, Wijffels RH, Martens DE (2018) The impact of day length on cell division and efficiency of light use in a starchless mutant of Tetradesmus obliquus. Algal Res 31:387–394
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 81:629–636
Liu A-Y, Chen W, Zheng L-L, Song L-R (2011) Identification of high-lipid producers for biodiesel production from forty three green algal isolates in China. Prog Nat Sci 21:269–276
Liu Z-Y, Wang G-C, Zhou B-C (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722
Luciana WT, Alba LG, Brito RMS, Santos AR, Cortez FZ, Pusceddu FH, Landulfo AC, Marcos SJ, Pacheco TT, Pereira CDS (2014) Safflower oil: an integrated assessment of phytochemistry, antiulcerogenic activity, and rodent and environmental toxicity. Rev Bras Farm 24:538–544
Maeda Y, Yoshino T, Matsunaga T, Matsumoto M, Tanaka T (2018) Marine microalgae for production of biofuels and chemicals. Curr Opin Biotech 50:111–120
Montoya C, Cochard B, Flori A, Cros D, Lopes R, Cuellar T, Espeout S, Syaputra I, Villeneuve P, Pina M, Ritter E, Leroy T, Billotte N (2014) Genetic architecture of palm oil fatty acid composition in cultivated oil palm (Elaeis guineensis Jacq.) compared to its wild relative E. oleifera (H.B.K) Cortés, PLoS One 9:e95412
Mostafa SSM (2012) Microalgal biotechnology: prospects and applications. In: Dhal NK, Sahu SC (eds) Plant science. InTech, London, pp 275–314
Müller A, Ringseis R, Düsterloh K, Gahler S, Eder K, Steinhart H (2005) Detection of conjugated dienoic fatty acids in human vascular smooth muscle cells treated with conjugated linoleic acid. Biochim Biophys Acta 1737:145–151
Najm S, Löfqvist C, Hellgren G, Engström E, Lundgren P, Hård AL, Lapillonne A, Sävman K, Nilsson AK, Andersson MX, Smith LEH, Hellström A (2017) Effects of a lipid emulsion containing fish oil on polyunsaturated fatty acid profiles, growth and morbidities in extremely premature infants: a randomized controlled trial. Clin Nutr ESPEN 20:17–23
Nascimento IA, Marques SSI, Cabanelas ITD, Pereira SA, Druzian JI, de Souza CO, Vich DV, de Carvalho GC, Nascimento MA (2013) Screening microalgae strains for biodiesel production: lipid productivity and estimation of fuel quality based on fatty acids profiles as selective criteria. BioEnergy Res 6:1–13
Nichols HW (1973) Growth media – freshwater. In: Stein JR (ed) Handbook of phycological methods, culture methods and growth measurements. Cambridge University Press, Cambridge, pp 7–24
Nilsson AK, Löfqvist C, Najm S, Hellgren G, Sävman K, Andersson MX, Smith LEH, Hellström A (2018) Long-chain polyunsaturated fatty acids decline rapidly in milk from mothers delivering extremely preterm indicating the need for supplementation. Acta Paediatr 107:1020-1027
Palamar-Mordvintseva GM (1982) Opredelitelj presnovodnikh vodoroslei SSSR. Zelenye vodorosli, klass konjugaty, porjadok desmidievye. Nauka Leningradskoe otdelenie, Leningrad
Park JBK, Craggs RJ, Shilton AN (2011) Wastewater treatment high rate algal ponds for biofuel production. Bioresource Techn 102:35–42
Pascual G, Avgustinova A, Mejetta S, Martín M, Castellanos C, Attolini CS-O, Berenguer A, Prats N, Toll A, Hueto JA, Bescós C, Di Croce L, Benitah SA (2017) Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature 541:41–45
Płazcek M, Patyna A, Witczak S (2017): Technical evaluation of photobioreactors for microalgae cultivation. In: Wzorek M, Królczyk G, Król A (eds) E3S web of conferences, Volume 19. Polanica-Zdrój, Poland, pp 1–10
Porter NA, Caldwell SE, Mills KA (1995) Mechanisms of free radical oxidation of unsaturated lipids. Lipids 30:277–290
Ravi L, Krishnan K (2017) Cytotoxic potential of N-hexadecanoic acid extracted from Kigelia pinnata leaves. Asian J Cell Biol 12:20–27
Richmond A (ed) (2004) Handbook of microalgal culture: biotechnology and applied phycology. Blackwell Publishing Ltd., Oxford
Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2008) Microalgae for oil: strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102:100–112
Sakthivel R, Elumalai S, Arif MM (2011) Microalgae lipid research, past, present: a critical review for biodiesel production, in the future. J Exp Sci 2:29–49
Santos LMA, Santos MF (2004) The Coimbra culture collection of algae (ACOI). Nova Hedwigia 79:39–47
Shifrin NS, Chisholm SW (1981) Phytoplankton lipids: interspecific differences and effects of nitrate, silicate and light-dark cycles. J Phycol 17:374–384
Snow AA, Smith VH (2012) Genetically engineered algae for biofuels: a key role for ecologists. BioScience 62:765–768
Song M, Pei H, Hua W, Maa G (2013) Evaluation of the potential of 10 microalgal strains for biodiesel production. Bioresour Technol 141:245–251
Spijkerman E, Garcia-Mendoza E, Matthijs HCP, van Hunnik E, Coesel PFM (2004) Negative effects of P-buffering and pH on photosynthetic activity of planktonic desmid species. Photosynthetica 42:49–57
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96
Stamenković M, Cvijan M (2008a) High tolerance to water pollution in Cosmarium boitierense Kouwets and Staurastrum bloklandie Coesel et Joosten taxa recorded for the first time from the Balkan Peninsula. Algol Studies 127:83–94
Stamenković M, Cvijan M (2008b) Some new and interesting ecological observations on desmids from the province of Vojvodina (northern Serbia). Biologia 63:921–927
Stamenković M, Hanelt D (2011) Growth and photosynthetic characteristics of several Cosmarium strains (Zygnematophyceae, Streptophyta) isolated from various geographic regions under a constant light-temperature regime. Aquatic Ecol 45:455–472
Stamenković M, Hanelt D (2013a) Adaptation of growth and photosynthesis to certain temperature regimes is an indicator for the geographic distribution of several Cosmarium strains (Zygnematophyceae, Streptophyta). Eur J Phycol 48:116–127
Stamenković M, Hanelt D (2013b) Protection strategies of several Cosmarium strains (Zygnematophyceae, Streptophyta) isolated from various geographic regions against excessive photosynthetically active radiation. Photochem Photobiol 89:900–910
Stamenković M, Woelken E, Hanelt D (2014) Ultrastructure of Cosmarium strains (Zygnematophyceae, Streptophyta) collected from various geographic locations shows species-specific differences both at optimal and stress temperatures. Protoplasma 251:1491–1509
Stamenković M, Hanelt D (2017) Geographic distribution and ecophysiological adaptations of desmids (Zygnematophyceae, Streptophyta) in relation to PAR, UV radiation and temperature: a review. Hydrobiologia 787:1–26
Steinhoff FS, Karlberg M, Graeve M, Wulff A (2014) Cyanobacteria in Scandinavian coastal waters – a potential source for biofuels and fatty acids? Algal Res 5:42–51
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 2:258–267
Vidyashankar S, Gopal KSV, Swarnalatha GV, Kavitha MD, Chauhan VS, Ravi R, Bansal AK, Singh R, Pande A, Ravishankar GA, Sarada R (2015) Characterization of fatty acids and hydrocarbons of chlorophycean microalgae towards their use as biofuel source. Biomass Bioenergy 77:75–91
Vigani M, Parisi C, Rodríguez-Cerezo E, Barbosa MJ, Sijtsma L, Ploeg M, Enzing C (2015) Food and feed products from micro-algae: market opportunities and challenges for the EU. Trends Food Sci Technol 42:81–92
von Alvensleben N, Stookey K, Magnusson M, Heimann K (2013) Salinity tolerance of Picochlorum atomus and the use of salinity for contamination control by the freshwater cyanobacterium Pseudanabaena limnetica. PLoS One 8:e0063569
von Schwartzenberg K, Bornfleth S, Lindner AC, Hanelt D (2013) The Microalgae and Zygnematophyceae Collection Hamburg (MZCH) – living cultures for research on rare streptophytic algae. Algol Studies 142:77–107
Wacker A, Piepho M, Harwood JL, Guschina IA, Arts MT (2016) Light-induced changes in fatty acid profiles of specific lipid classes in several freshwater phytoplankton species. Front Plant Sci 7:264
Wang J-K, Seibert M (2017) Prospects for commercial production of diatoms. Biotechnol Biofuels 10:16
Yoo C, Jun S, Lee J, Ahn C, Oh H (2010) Selection of microalgae for lipid production under high levels carbon dioxide. Bioresour Technol 101:571–574
Yu W-L, Ansari W, Schoepp NG, Hannon MJ, Mayfield SP, Burkart MD (2011) Modifications of the metabolic pathways of lipid and triacylglycerol production in microalgae. Microb Cell Factories 10:91
Acknowledgements
The authors thank M. Hedblom, J. Pearce and G. Knutsson for valuable support in laboratory.
Funding
This research project is supported by the University of Gothenburg, and by the research grant of the Swedish Institute provided to M. Stamenković (SI No. 02390/2016). M. Stamenković is also funded by the project No. 173018 of the Ministry of Education, Science and Technological Development of the Republic of Serbia.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Stamenković, M., Steinwall, E., Nilsson, A.K. et al. Desmids (Zygnematophyceae, Streptophyta) as a promising freshwater microalgal group for the fatty acid production: results of a screening study. J Appl Phycol 31, 1021–1034 (2019). https://doi.org/10.1007/s10811-018-1598-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-018-1598-8