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Biosynthesis of polyunsaturated fatty acids by two newly cold-adapted Egyptian marine yeast

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Abstract

The widespread awareness of polyunsaturated fatty acids (PUFAs) benefits for human health has increased the need for their commercial production. Two oleaginous yeast were isolated from the Mediterranean Sea fish and Red Sea fish Epinephelus aeneus and E. areolatus, respectively. These marine candidates were identified by MALDI-TOF/MS biotyper® as Lodderomyces elongisporus and Rhodotorula mucilaginosa. The effect of incubation temperature (7, 15, and 26 °C) and glucose concentration (3% and 8%) on their lipids content were investigated using Sulfo-Phospho-Vanillin (SPV) assay. Their intercellular lipids were visualized by fluorescence microscope using Nile-Red dye. L. elongisporus and R. mucilaginosa produced 20.04% and 26.79% of Linoleic acid, respectively, on normal Basal-Defatted Medium (BDM). Linoleic acid (21.4–22.7%) and α-Linolenic acid (7.5–10.8%) were produced by R. mucilaginosa and L. elongisporus, on normal BDM at 15 °C. High-Glucose BDM induced a positive effect on the total lipids production that reached its maximum of 48% and 54% by R. mucilaginosa and L. elongisporus, respectively, grown at 15 °C. Remarkably, 12.12% of long-chain 15-Docosenoic acid (C22:1) and 21.49% of Tricosanoic acid (C23:0) were detected in the FAs profile of L. elongisporus, when grown on normal BDM at 26 °C. The present study is the first one reporting the FAs profile of the Egyptian Marine L. elongisporus, and its capability to accumulate high amounts of lipids under appropriate fermentation conditions; thus, it could be considered for scaling up production.

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References

  • Abd Elrazak A, Ward AC, Glassey J (2013) Polyunsaturated fatty acid production by marine bacteria. Bioprocess Biosyst Eng 36:1641–1652

    Article  CAS  PubMed  Google Scholar 

  • Ageitos JM, Vallejo JA, Veiga-Crespo P, Villa TG (2011) Oily yeasts as oleaginous cell factories. Appl Microbiol Biotechnol 90:1219–1227

    Article  CAS  PubMed  Google Scholar 

  • Agustini BC, Silva LP, Bloch C et al (2014) Evaluation of MALDI-TOF mass spectrometry for identification of environmental yeasts and development of supplementary database. Appl Microbiol Biotechnol 98:5645–5654

    Article  CAS  PubMed  Google Scholar 

  • Ahmed SO, Nasser AA, Abbas RN et al (2021) Production of bioConcrete with improved durability properties using Alkaliphilic Egyptian bacteria. 3 Biotech 11:1–15

    Article  Google Scholar 

  • Amaretti A, Raimondi S, Sala M et al (2010) Single cell oils of the cold-adapted oleaginous yeast Rhodotorula glacialis DBVPG 4785. Microb Cell Fact 9:1–6

    Article  Google Scholar 

  • Axelsson M, Gentili F (2014) A single-step method for rapid extraction of total lipids from green microalgae. PLoS ONE 9:e89643

    Article  PubMed  PubMed Central  Google Scholar 

  • Bellou S, Triantaphyllidou I-E, Aggeli D et al (2016) Microbial oils as food additives: recent approaches for improving microbial oil production and its polyunsaturated fatty acid content. Curr Opin Biotechnol 37:24–35

    Article  CAS  PubMed  Google Scholar 

  • Beopoulos A, Cescut J, Haddouche R et al (2009) Yarrowia lipolytica as a model for bio-oil production. Prog Lipid Res 48:375–387

    Article  CAS  PubMed  Google Scholar 

  • Botha A, Kock JL (1993) Application of fatty acid profiles in the identification of yeasts. Int J Food Microbiol 19:39–51

    Article  CAS  PubMed  Google Scholar 

  • Butinar L, Strmole T, Gunde-Cimerman N (2011) Relative incidence of ascomycetous yeasts in arctic coastal environments. Microb Ecol 61:832–843

    Article  PubMed  Google Scholar 

  • Cheng Y-S, Zheng Y, VanderGheynst JS (2011) Rapid quantitative analysis of lipids using a colorimetric method in a microplate format. Lipids 46:95–103

    Article  CAS  PubMed  Google Scholar 

  • Chintalapati S, Kiran M, Shivaji S (2004) Role of membrane lipid fatty acids in cold adaptation. Cell Mol Biol (noisy-Le-Grand) 50:631–642

    CAS  Google Scholar 

  • Connor WE, Connor SL (2007) The importance of fish and docosahexaenoic acid in Alzheimer disease. Am J Clin Nutr 85(4):929–930

    Article  CAS  PubMed  Google Scholar 

  • De Garcia V, Brizzio S, Libkind D et al (2007) Biodiversity of cold-adapted yeasts from glacial meltwater rivers in Patagonia, Argentina. FEMS Microbiol Ecol 59:331–341

    Article  PubMed  Google Scholar 

  • Dien BS, Slininger PJ, Kurtzman CP et al (2016) Identification of superior lipid producing Lipomyces and Myxozyma yeasts. AIMS Environ Sci 3:1–20

    Article  CAS  Google Scholar 

  • Dikma-Technologies (2021) Fames (marine oil standard). Retrieved from: http://www.dikmatech.com/Application/show/id/186

  • Diniz Rufino R, Moura de Luna J, de Campos Takaki GM, Asfora Sarubbo L (2014) Characterization and properties of the biosurfactant produced by Candida lipolytica UCP 0988. Electron J Biotechnol 17:6–6

    Google Scholar 

  • El-Baz AF, Shetaia YM, Elkhouli RR (2011) Xylitol production by Candida tropicalis under different statistically optimized growth conditions. Afr J Biotech 10:15353–15363

    Article  CAS  Google Scholar 

  • El-Baz AF, Sorour NM, Shetaia YM (2016) Trichosporon jirovecii–mediated synthesis of cadmium sulfide nanoparticles. J Basic Microbiol 56:520–553

    Article  CAS  PubMed  Google Scholar 

  • El-Baz AF, El-Enshasy HA, Shetaia YM et al (2018) Semi-industrial scale production of a new yeast with probiotic traits, Cryptococcus sp. YMHS, isolated from the Red Sea. Probiotics Antimicrob Proteins 10:77–88

    Article  CAS  PubMed  Google Scholar 

  • Funk CD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294:1871–1875

    Article  CAS  PubMed  Google Scholar 

  • Galán B, Santos-Merino M, Nogales J, et al (2020) Microbial oils as nutraceuticals and animal feeds. In: Health consequences of microbial interactions with hydrocarbons, oils, and lipids. pp 401–445

  • Greenspan P, Mayer EP, Fowler SD (1985) Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100:965–973

    Article  CAS  PubMed  Google Scholar 

  • Gupta A, Vongsvivut J, Barrow CJ, Puri M (2012) Molecular identification of marine yeast and its spectroscopic analysis establishes unsaturated fatty acid accumulation. J Biosci Bioeng 114:411–417

    Article  CAS  PubMed  Google Scholar 

  • Guschina IA, Harwood JL (2006) Lipids and lipid metabolism in eukaryotic algae. Prog Lipid Res 45:160–186

    Article  CAS  PubMed  Google Scholar 

  • Johansen PG, Owusu-Kwarteng J, Parkouda C et al (2019) Occurrence and importance of yeasts in indigenous fermented food and beverages produced in Sub-Saharan Africa. Front Microbiol 10:1789

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones E, Sakayaroj J, Suetrong S et al (2009) Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers 35:187

    Google Scholar 

  • Jostensen J-P, Landfald B (1997) High prevalence of polyunsaturated-fatty-acid producing bacteria in arctic invertebrates. FEMS Microbiol Lett 151:95–101

    Article  CAS  Google Scholar 

  • Kimura K, Yamaoka M, Kamisaka Y (2004) Rapid estimation of lipids in oleaginous fungi and yeasts using Nile red fluorescence. J Microbiol Methods 56:331–338

    Article  CAS  PubMed  Google Scholar 

  • Knight JA, Anderson S, Rawle JM (1972) Chemical basis of the sulfo-phospho-vanillin reaction for estimating total serum lipids. Clin Chem 18:199–202

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Du W, Liu D (2008) Perspectives of microbial oils for biodiesel production. Appl Microbiol Biotechnol 80:749–756

    Article  CAS  PubMed  Google Scholar 

  • Li M, Liu G-L, Chi Z, Chi Z-M (2010) Single cell oil production from hydrolysate of cassava starch by marine-derived yeast Rhodotorula mucilaginosa TJY15a. Biomass Bioenerg 34:101–107

    Article  CAS  Google Scholar 

  • Ma C, Liu J, Zhou T et al (2015) Identification and phylogenetic analysis of two marine petroleum-degrading yeasts from South China Sea Offshore based on magnetic nanoparticles extraction. J Bionanosci 9:215–221

    Article  CAS  Google Scholar 

  • Margesin R (2009) Effect of temperature on growth parameters of psychrophilic bacteria and yeasts. Extremophiles 13:257–262

    Article  PubMed  Google Scholar 

  • Marklein G, Josten M, Klanke U et al (2009) Matrix-assisted laser desorption ionization-time of flight mass spectrometry for fast and reliable identification of clinical yeast isolates. J Clin Microbiol 47:2912–2917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marvin LF, Roberts MA, Fay LB (2003) Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in clinical chemistry. Clin Chim Acta 337:11–21

    Article  CAS  PubMed  Google Scholar 

  • Mishra SK, Suh WI, Farooq W et al (2014) Rapid quantification of microalgal lipids in aqueous medium by a simple colorimetric method. Biores Technol 155:330–333

    Article  CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2002) Lipid production by Yarrowia lipolytica growing on industrial glycerol in a single-stage continuous culture. Biores Technol 82:43–49

    Article  CAS  Google Scholar 

  • Papanikolaou S, Aggelis G (2019) Sources of microbial oils with emphasis to Mortierella (Umbelopsis) isabellina fungus. World J Microbiol Biotechnol 35:63

    Article  PubMed  Google Scholar 

  • Parolini C (2020) Marine n-3 polyunsaturated fatty acids: Efficacy on inflammatory-based disorders. Life Sci 263:118591

    Article  CAS  PubMed  Google Scholar 

  • Poli JS, Dallé P, Senter L et al (2013) Fatty acid methyl esters produced by oleaginous yeast Yarrowia lipolytica QU21: an alternative for vegetable oils. Revista Brasileira de Biociências 11

  • Qiu X, Xie X, Meesapyodsuk D (2020) Molecular mechanisms for biosynthesis and assembly of nutritionally important very long chain polyunsaturated fatty acids in microorganisms. Progr Lipid Res 79:101047

    Article  CAS  Google Scholar 

  • Ratledge C (1982) Microbial oils and fats: An assessment of their commercial potential [algae, yeasts, fungi]. Progr Ind Microbiol 16:119–206

    CAS  Google Scholar 

  • Ratledge C (2002) Regulation of lipid accumulation in oleaginous microorganisms. Biochem Soc Trans 30:1047–1050

    Article  CAS  PubMed  Google Scholar 

  • Restek-Corporation (2018) Fames (marine oil standard) on famewax. Retrieved from: http://www.restek.com/chromatogram/view/GC-FF00568

  • Rossi M, Buzzini P, Cordisco L et al (2009) Growth, lipid accumulation, and fatty acid composition in obligate psychrophilic, facultative psychrophilic, and mesophilic yeasts. FEMS Microbiol Ecol 69:363–372

    Article  CAS  PubMed  Google Scholar 

  • Ryan J, Farr H, Visnovsky S et al (2010) A rapid method for the isolation of eicosapentaenoic acid-producing marine bacteria. J Microbiol Methods 82:49–53

    Article  CAS  PubMed  Google Scholar 

  • Satyanarayana T, Kunze G (2009) Yeast biotechnology: diversity and applications. Springer

    Book  Google Scholar 

  • Sitepu IR, Sestric R, Ignatia L et al (2013) Manipulation of culture conditions alters lipid content and fatty acid profiles of a wide variety of known and new oleaginous yeast species. Biores Technol 144:360–369

    Article  CAS  Google Scholar 

  • Skerratt JH, Bowman JP, Nichols PD (2002) Shewanella olleyana sp. nov. A marine species isolated from a temperate estuary which produces high levels of polyunsaturated fatty acids. Int J Syst Evol Microbiol 52:2101–2106

    CAS  PubMed  Google Scholar 

  • Sorour N, Karboune S, Saint-Louis R, Kermasha S (2012a) Lipase-catalyzed synthesis of structured phenolic lipids in solvent-free system using flaxseed oil and selected phenolic acids as substrates. J Biotechnol 158:128–136

    Article  CAS  PubMed  Google Scholar 

  • Sorour N, Karboune S, Saint-Louis R, Kermasha S (2012b) Enzymatic synthesis of phenolic lipids in solvent-free medium using flaxseed oil and 3, 4-dihydroxyphenyl acetic acid. Process Biochem 47:1813–1819

    Article  CAS  Google Scholar 

  • Stokes J, Tu R, Peters M et al (2020) Omega-3 fatty acids from algae produced biodiesel. Algal Res 51:102047

    Article  Google Scholar 

  • Troiano D, Orsat V, Dumont MJ (2020) Status of filamentous fungi in integrated biorefineries. Renew Sustain Energy Rev 117:109472

    Article  CAS  Google Scholar 

  • Wang L, Chi Z, Wang X et al (2007) Diversity of lipase-producing yeasts from marine environments and oil hydrolysis by their crude enzymes. Ann Microbiol 57:495–501

    Article  CAS  Google Scholar 

  • Wang J, Li R, Lu D et al (2009) A quick isolation method for mutants with high lipid yield in oleaginous yeast. World J Microbiol Biotechnol 25:921–925

    Article  CAS  Google Scholar 

  • Wang Q, Cui Y, Sen B et al (2017) Characterization and robust nature of newly isolated oleaginous marine yeast Rhodosporidium spp. from coastal water of Northern China. AMB Express 7:1–13

    Article  Google Scholar 

  • Wieser A, Schneider L, Jung J, Schubert S (2012) MALDI-TOF/MS in microbiological diagnostics-identification of microorganisms and beyond (mini review). Appl Microbiol Biotechnol 93:965–974

    Article  CAS  PubMed  Google Scholar 

  • Xu H, Turchini GM, Francis DS et al (2020) Are fish what they eat? A fatty acid’s perspective. Progr Lipid Res 80:101064

    Article  CAS  Google Scholar 

  • Xue Z, Sharpe PL, Hong S-P et al (2013) Production of omega-3 eicosapentaenoic acid by metabolic engineering of Yarrowia lipolytica. Nat Biotechnol 31:734–740

    Article  CAS  PubMed  Google Scholar 

  • Yarrow D (1998) Methods for the isolation, maintenance and identification of yeasts. The yeasts. Elsevier, pp 77–100

    Chapter  Google Scholar 

  • Yazawa K (1996) Production of eicosapentaenoic acid from marine bacteria. Lipids 31:S297–S300

    Article  CAS  PubMed  Google Scholar 

  • You L, Li M, Wang Z et al (2017) Influences of a Lodderomyces elongisporus strain on fermentation of strong-flavored liquor. Food Ferment Ind 43:9–13

    Google Scholar 

  • Zhu M, Yu L, Liu Z, Xu H (2004) Isolating Mortierella alpina strains of high yield of arachidonic acid. Lett Appl Microbiol 39:332–335

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Food Safety Organization, Cairo, Egypt

    Amera Adel

  2. Département of Industrial Biotechnology, Genetic Engineering and Biotechnology Research Institute, University of Sadat City, Sadat City, 22857/79, Egypt

    Ashraf El-Baz & Noha Mohamed Sorour

  3. Department of Microbiology, Faculty of Science, Ain Shams University, Cairo, Egypt

    Yousseria Shetaia

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  1. Amera Adel
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  2. Ashraf El-Baz
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  3. Yousseria Shetaia
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  4. Noha Mohamed Sorour
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Correspondence to Noha Mohamed Sorour.

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Adel, A., El-Baz, A., Shetaia, Y. et al. Biosynthesis of polyunsaturated fatty acids by two newly cold-adapted Egyptian marine yeast. 3 Biotech 11, 461 (2021). https://doi.org/10.1007/s13205-021-03010-4

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