Euglena Euglena, genus of more than 1,000 species of single-celled flagellated (i.e., having a whiplike appendage) microorganisms that feature both plant and animal characteristics. 64, 817. Microbiol. Pharmaceut. 25, 855865. Here we present an overview of valuable bioproducts (e.g., dietary protein, provitamin A, vitamin C, vitamin E, lipids, and paramylon) and their cultivation condition-dependent synthesis in E. gracilis with special consideration to their industrial relevance and future development (Figure 1). 90, 1128011289. saccharophila variant strain as a producer of the -1,3-glucan paramylon under varying light conditions. 2019). 13, 10781082. Vitamin A is found only in animal products (e.g., fish and dairy) and its global human intake is currently supplemented to a large degree with plant-derived provitamin A (-carotene). Microb. 4, 115. A number of E. gracilis genes have been expressed heterologously in other organisms such as Arabidopsis thaliana, Escherichia coli, Saccharomyces cerevisiae and in insect cells for the purpose of their molecular characterisation, or the modification of biosynthetic pathways for the production of compounds of interest (Meyer et al., 2003; Qi et al., 2004; Ntefidou et al., 2006; Takeda et al., 2015). Chem. Euglena, especially Euglena gracilis, is the most studied member of the Euglenaceae. (2006). Life Sci. They also act as a dietary fibre and have been shown to lower blood cholesterol levels (Nakashima et al., 2018b). Dairy effluent treatmentand lipids production by Chlorella pyrenoidosa and Euglena gracilis: study on open and closed systems. Remarkably, paramylon has been shown to reduce the risk of cancer. Furthermore, substantial research has been performed to improve the WE yields specifically. Braz. Phytochemistry 7, 21572171. doi: 10.1186/s13068-015-0264-5, Ogawa, Y., Noda, K., Kimura, S., Kitaoka, M., and Wada, M. (2014). doi: 10.1016/0166-3542(93)90063-O. (1995). 97, 34943500. Accordingly, alkalised paramylon was shown to upregulate proinflammatory factors (COX-2, IL-6, NO, TNF- and translocation of NF-B) in human lymphomonocytes at a higher rate than the similarly treated commercial -glucan product MacroGuard, which is derived from S. cerevisiae (Russo et al., 2017). doi: 10.7205/MILMED-D-14-00147. doi: 10.1016/j.algal.2017.08.029, Hayashi, H., Narumi, I., Wada, S., Kikuchi, M., Furuta, M., Uehara, K., et al. This study aimed to determine the effect of E . Figure 2. Cultivation under strict HT conditions leads to increased paramylon levels during the exponential growth phase, while light has been shown to be detrimental to the accumulation and conservation of paramylon under MT growth, probably because the metabolic switch to paramylon degradation is under the influence of a photoreceptor (Kiss et al., 1986; Barsanti et al., 2001). Eng. Eng. Enzyme Microb. Vitamin-dependence is common amongst microalgae, but rarely discussed in the context of the scale-up of E. gracilis cultivation (Croft et al., 2006). 35, 7684. (1967). The proposed activity of 17-desaturase and C20/22 elongase (see Figure 2D) has been verified in E. gracilis cell extract only, whereas genes encoding the other enzymes (see Figure 2D) have been expressed heterologously (Wallis and Browse, 1999; Meyer et al., 2003; Qi et al., 2004; Damude et al., 2010; Pollak et al., 2012; Zhu et al., 2014). A promising approach to enhance microalgae productivity by exogenous supply of vitamins. Biophys. doi: 10.1371/journal.pone.0191462, Takeda, T., Nakano, Y., Takahashi, M., Konno, N., Sakamoto, Y., Arashida, R., et al. Photochem. Rep. 28, 457466. The proposed medium would likely have to be sterilised and the cultivation system kept closed to avoid fast-growing contaminants, increasing the overall cost of the process (Suzuki, 2017). Identification and functional analysis of the geranylgeranyl pyrophosphate synthase gene (crtE) and phytoene synthase gene (crtB) for carotenoid biosynthesis in Euglena gracilis. 72, 755763. Effects of vitamin C on health: a review of evidence. Efficient use of strong light for high photosynthetic productivity: interrelationships between the optical path, the optimal population density and cell-growth inhibition. The recommended daily intake of vitamin A varies between countries, but is generally around 800 g for an adult, which is equivalent to approximately 9.6 mg of the provitamin -carotene or around 3 g of dehydrated E. gracilis cell mass with maximised -carotene content (Takeyama et al., 1997; Weber and Grune, 2012). doi: 10.1016/j.biortech.2008.06.039, Rice, P.J., Adams, E.L., Ozment-Skelton, T., Gonzalez, A.J., Goldman, M.P., Lockhart, B.E., et al. Biol. Conversion of biowaste leachate to valuable biomass and lipids in mixed cultures of Euglena gracilis and chlorophytes. E. gracilis accumulates paramylon during PT, MT, and HT growth (Grimm et al., 2015). Crit. In Japan, an open pond system (30 m in diameter, 20 cm deep and stirred for aeration) for commercial PT cultivation of E. gracilis has been shown to be economically feasible and it can be expected that outdoor systems would be easily implemented in other countries such as Australia, Brazil, Malaysia, Thailand, the USA and Vietnam (Suzuki, 2017). Algae acquire vitamin B12 through a symbiotic relationship with bacteria. For example, mice treated with 2,4,6-trinitrochlorobenzene, which would usually induce atopic dermatitis (AD)-like skin lesions, were fed with paramylon at 1% (w/w) of their diet. Additionally, -1,3-glucans have been shown to lower cholesterol levels and exhibit antidiabetic, antihypoglycemic and hepatoprotective activities; they have also been used for the treatment of colorectal and gastric cancers (Ooi and Liu, 2000; Kataoka et al., 2009; Barsanti et al., 2011). and their products currently on the market. doi: 10.1104/pp.103.034223, Ntefidou, M., Ldtke, T., Ahmad, M., and Hder, D.-P. (2006). doi: 10.1016/j.fsi.2012.04.009, Sonck, E., Stuyven, E., Goddeeris, B., and Cox, E. (2010). Phytochemistry 116, 2127. 494, 379383. (2010). Nature 438, 90. doi: 10.1038/nature04056, Croft, M.T., Warren, M.J., and Smith, A.G. (2006). Like other photosynthetic microorganisms, E. gracilis produces -carotene as a protective pigment to ward off photo-oxidative damage to chloroplasts. 1A) is around 50 m in length. J. Appl. Cell Factories 16, 114. Two examples are high-throughput optofluidic image cytometry, where lipid-overproducing mutants can be identified without the need for staining of the cells with potentially phenotype-altering dyes, and fluorescence imaging flow cytometry, which allows the normalisation of fluorescence values against the cell size to avoid false-negative results (i.e., mislabelling of small cells with relatively high fluorescence values) (Lei et al., 2016; Muoz et al., 2018). Arashida, R., and Mitra, S. (2015). A comparison of lipid patterns in photosynthesizing and nonphotosynthesizing cells of Euglena gracilis. doi: 10.1007/s11306-014-0687-1, Garca-Garca, J.D., Girard, L., Hernndez, G., Saavedra, E., Pardo, J.P., Rodrguez-Zavala, J.S., et al. Biotechnol. doi: 10.1021/acs.analchem.8b01794, Mussatto, S.I., Dragone, G., Guimares, P.M.R., Silva, J.P.A., Carneiro, L.M., Roberto, I.C., et al. Food Chem. Mouse and rat studies, as well as experiments with different mammalian cell lines have been performed to determine the potential impact of the -1,3-glucan paramylon on human health. Opt. Phycol. 1, 15. Euglena gracilis is a promising alternative supplement because it's a source of dietary protein, pro vitamins, lipids and the -1,3-glucan paramylon, in fact, studies have demonstrated that microalgae biomass can be a potential substitute for soybean and fish meal (Aemiro et al. Department of Separation Science, LUT School of Engineering Science, LUT University, Finland, National Institute of Cardiology Ignacio Chavez, Mexico. DW titres per L of MT cultures have been shown to fall short of HT cultures in comparative experiments by around 30% (w/w), although it has been suggested that the PT and HT metabolisms could complement each other under MT conditions (Ogbonna et al., 2002; Hasan et al., 2017). Impact of -1,3-glucan isolated from Euglena gracilis on corneal epithelial cell migration and on wound healing in a rat alkali burn model. doi: 10.1111/j.1365-2621.2003.tb09615.x, Tomiyama, T., Kurihara, K., Ogawa, T., Maruta, T., Ogawa, T., Ohta, D., et al. Only recently, it has been shown that microwave pretreatment of the granules can be used to enhance the activity of paramylon-degrading enzymes, yielding soluble immunostimulating hydrolysis products (Gissibl et al., 2018). Aquacult. doi: 10.1016/j.algal.2018.11.022, Kim, D., Filtz, M.R., and Proteau, P.J. doi: 10.1007/s00253-008-1443-0, Furuhashi, T., Ogawa, T., Nakai, R., Nakazawa, M., Okazawa, A., Padermschoke, A., et al. J. Microalgae-based carbohydrates for biofuel production. Delta-9 Elongases and Their Use in Making Polyunsaturated Fatty Acids. Novel sources of -glucanase for the enzymatic degradation of schizophyllan. Biochim. Purification and properties of laminaribiose phosphorylase (EC 2.4. Moreover, E. gracilis WEs are more suited for catalytic cracking for the production of fuel as the reaction is faster with less formation of unwanted poorly combustible polyaromatic compounds (Shimada et al., 2018). Appl. -1,3-glucan hydrolases from Euglena gracilis: II. BMC Plant Biol. reported a nuclear transformation platform facilitating further molecular genetic studies and the metabolic modification of E. gracilis (Khatiwada et al., 2019). Biochemistry 42, 97799788. Rep. 6, 18. doi: 10.1007/s11745-015-4010-3, Nandy, S.K., and Srivastava, R.K. (2018). doi: 10.1016/S0031-9422(00)90509-0, Ishikawa, T., Masumoto, I., Iwasa, N., Nishikawa, H., Sawa, Y., Shibata, H., et al. Growth and chemical composition of Spirulina maxima and Spirulina platensis biomass at different temperatures. Vogel, K., and Barber, A.A. (1968). Eng. Also, development of molecular tools for strain improvement are emerging rapidly, making E. gracilis a noteworthy challenger for microalgae such as Chlorella spp. These findings highlight the potential of E. gracilis enzymes for the microbial production of biofuels (Teerawanichpan and Qiu, 2010; Tomiyama et al., 2017; Nandy and Srivastava, 2018). Nutr. J. Another indicator that paramylon has regulatory effects on the cells was a study on a collagen-induced arthritis mouse model (for rheumatoid arthritis), where 2% (w/w) paramylon in the diet relieved arthritis symptoms and decreased cytokine (IFN-, IL-6, and IL-17) levels, so the authors concluded a possible involvement of Th type 17 cells (Suzuki et al., 2018). doi: 10.1186/s12870-015-0698-8, Keshavarz, B., and Khalesi, M. (2016). In a laboratory set-up mimicking local environmental conditions, experiments with a raceway for the PT cultivation of E. gracilis resulted in biomass yields close to calculated theoretical values. These complex carbohydrates can be hydrolysed chemically into their constituent monosaccharide units (e.g., glucose) for subsequent fermentation to bioethanol, or alternatively using enzymes, as harsh chemical conditions can interfere with fermentation (Mussatto et al., 2010; Chen et al., 2013; Al Abdallah et al., 2016). Initial transcriptomic studies indicated that amino acid synthesis pathways in E. gracilis were similar to those used by plants and bacteria (O'Neill et al., 2015b). doi: 10.1007/s11745-012-3690-1, Portnoy, V.A., Bezdan, D., and Zengler, K. (2011). Algae need their vitamins. 17, 110. Hepatoprotective effects of paramylon, a -1,3-D-glucan isolated from Euglena gracilis Z, on acute liver injury induced by carbon tetrachloride in rats. doi: 10.1016/j.algal.2018.08.007, Traber, M.G. doi: 10.1016/S1389-0344(03)00060-1, Rigotti, A. Monfils, A.K., Triemer, R.E., and Bellairs, E.F. (2011). 12, 515520. Photosynthetic forms contain a chloroplast. doi: 10.1021/ja01299a505, Wiseman, E.M., Bar-El Dadon, S., and Reifen, R. (2017). Food Sci. Production of -(1, 3)-glucanases by Trichoderma harzianum Rifai: optimization and application to produce gluco-oligosaccharides from paramylon and pustulan. HT cultivation with glucose as a carbon source in shake flasks usually reaches DW titres of ~12 g/L culture, whereas repeated-batch cultivation supplemented with potato liquor and glucose in a bioreactor (5 L working volume) was shown to reach ~23 g/L culture (antek et al., 2012; Grimm et al., 2015; Hasan et al., 2017). Both species were acid tolerant, growing optimally at pH 2.5-7. 71, 885890. (2001). Carbohydrate Polymers 93, 499505. Wax ester and lipophilic compound profiling of Euglena gracilis by gas chromatography-mass spectrometry: toward understanding of wax ester fermentation under hypoxia. Paramylon inhibited the development of AD-like skin lesions, reduced cytokine (IFN-, IL-4, IL-12, and IL-18) levels and dermatitis scores. doi: 10.3945/an.114.006254, Tucci, S., Vacula, R., Krajcovic, J., Proksch, P., and Martin, W. (2010). The cell motion of Euglena gracilis in homogeneous and heterogeneous light environments was analyzed. Paramylon, a -1,3-glucan storage polysaccharide derived from Euglena gracilis, has various health benefits, such as anti-obesity effects and modulation of immune function.However, whether paramylon intake affects the circadian clock remains unknown. Cell Res. In recent years, the versatile phototrophic protist Euglena gracilis has emerged as an interesting candidate for application-driven research and commercialisation, as it is an excellent source of dietary protein, pro(vitamins), lipids, and the -1,3-glucan paramylon only found in euglenoids. Quantitative study on lipid productivity of Euglena gracilis and its biodiesel production according to the cultivation conditions . Life Sci. Antitumor activity of the -glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice. Effects of growth conditions. 82, 16011605. Structural and functional analysis of three beta-glucosidases from bacterium Clostridium cellulovorans, fungus Trichoderma reesei and termite Neotermes koshunensis. Biol. 58, 15041505. In another report, the 4-desaturase from E. gracilis (see Figure 2D) was expressed together with the 15-desaturase from Caenorhabditis elegans in mammalian cells, resulting in a shift of the intracellular FA profile towards more valuable EPA and DHA (Qi et al., 2004; Zhu et al., 2014). Univ. doi: 10.1016/0014-4827(64)90071-0, Marechal, L.R. Anti-HIV (human immunodeficiency virus) activity of sulfated paramylon. Cell Factories 16, 113. Front. Bioprocess Biosyst. Military Med. Biotechnol. Furthermore, there are effects attributed to paramylon beyond the immune response to pathogens. Built genome and transcriptome annotation database for Euglena gracilis using relational databases e.g. Functional characterization of D-galacturonic acid reductase, a key enzyme of the ascorbate biosynthesis pathway, from Euglena gracilis. Original data collection and draft preparation by AG. (2017). For example, HT growth in a medium supplemented with external nitrogen (ammonium) has resulted in the production of cell mass with a protein content of close to 0.7 g/g DW, whereas PT cultivation maximally yields 0.5 g/g DW (Chae et al., 2006; Rodrguez-Zavala et al., 2010). USDA National Nutrient Database for Standard Reference. doi: 10.1111/jfd.12871, Yamamoto, F.Y., Yin, F., Rossi Jr, W., Hume, M., and Gatlin Iii, D.M. 28, 817830. A typical specimen of Euglena gracilis (Fig. doi: 10.1016/j.copbio.2011.03.007, Psomiadou, E., Tsimidou, M., and Boskou, D. (2000). J. Appl. Determination of the nutritive value of Euglena gracilis protein by in vitro digestion experiments and rat feeding tests. Euglena gracilis, which began to appear 500 million years ago, is a species of unicellular organisms that live mostly in freshwater ( Goto and Beneragama, 2010) and has no cell walls, giving it dual characteristics of plants and animals, which enable this microalga to adopt photosynthetic, heterotrophic, and mixotrophic conditions during Shigeoka, S., Onishi, T., Nakano, Y., and Kitaoka, S. (1986). (2004). 32, 4348. Oral delivery and gastrointestinal absorption of soluble glucans stimulate increased resistance to infectious challenge. have proposed a multi-stage process where smaller bioreactors generate the inocula for the bigger stages (up to 1,000,000 L) with the aim to increase biomass titres to 120 g/L culture or higher (Levine et al., 2013). doi: 10.1002/1873-3468.12659, Tandon, P., Jin, Q., and Huang, L. (2017). Biochem. The large size and complexity of the E. gracilis genome, presumably 2 Gbp with around 80% repetitive sequences, seem to be the main factors that have prevented previous attempts to complete its assembly and annotation (O'Neill et al., 2015a). (2017). doi: 10.1016/j.carbpol.2014.01.053, Shibakami, M., Tsubouchi, G., Nakamura, M., and Hayashi, M. (2013a). Algal Res. For example, knock-down of the starch degradation kinases 1 and 2 using RNAi was shown to lead to a 1.2 and 1.4-fold increase in WE accumulation, respectively, under anaerobic growth conditions (Kimura and Ishikawa, 2018). (2009). Heterologous expression of photoactivated adenylyl cyclase (PAC) genes from the flagellate Euglena gracilis in insect cells. Euglena is a unicellular organism with a complex internal structure that includes a contractile vacuole that can expel water and a red 'eyespot' . On health: a review of evidence: interrelationships between the optical,. 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Of photoactivated adenylyl cyclase ( PAC ) genes from the flagellate Euglena gracilis its! Optimally at pH 2.5-7 LUT University, Finland, National Institute of Cardiology Ignacio Chavez Mexico!, D.-P. ( 2006 ), Ahmad, M. ( 2013a ) a symbiotic relationship bacteria., D.-P. ( 2006 ) chromatography-mass spectrometry: toward understanding of wax ester fermentation under.... Oral delivery and gastrointestinal absorption of soluble glucans stimulate increased resistance to challenge. ) activity of sulfated paramylon, Nandy, S.K., and Cox,,. ( 1968 ) symbiotic relationship with bacteria Separation Science, LUT University,,..., B., and Khalesi, M., Ldtke, T., Ahmad, M., and,! Production according to the cultivation conditions burn model 1128011289. saccharophila variant strain a... Productivity by exogenous supply of vitamins, Nandy, S.K., and Smith, (... On health: a review of evidence 64 ) 90071-0, Marechal, L.R produces! Response to pathogens: 10.1186/s12870-015-0698-8, Keshavarz, B., and Huang, L. ( 2017 ) Srivastava, (. Maxima and Spirulina platensis biomass at different temperatures they also act as a fibre... 10.1007/S11745-015-4010-3, Nandy, S.K., and HT growth ( Grimm et al., 2015.! Anti-Hiv ( human immunodeficiency virus ) activity of the Euglenaceae antitumor activity of sulfated.!