doi: 10.1099/00221287-133-1-25, Shimada, I., Nakamura, Y., Kato, S., Mori, R., Ohta, H., Suzuki, K., et al. However, -tocopherol is the main dietary form in countries where consumed vegetable oils derive predominantly from soy and corn (e.g., in the USA), leading to an insufficient intake of -tocopherol in these regions (Jiang et al., 2001; Rigotti, 2007; Traber, 2014). doi: 10.1023/A:1010573218863, Yasuda, K., Ogushi, M., Nakashima, A., Nakano, Y., and Suzuki, K. (2018). 38, 9951008. Technol. B Agricult. Microbiol. J. Vet. Yet, it is assumed that the conversion of -tocopherol to -tocopherol is the rate-limiting step in the pathway of plants (Fritsche et al., 2017). Med. Two alternative metabolic routes to -carotene have been identified biochemically or via transcriptomics in E. gracilis: the methylerythritol phosphate and the mevalonate pathway (Disch et al., 1998; Kim et al., 2004; O'Neill et al., 2015b). Exp. In a heterogeneous environment, the cells move into the red circle. Remarkably, paramylon has been shown to reduce the risk of cancer. doi: 10.1016/j.plantsci.2011.07.018, Mahapatra, D.M., Chanakya, H.N., and Ramachandra, T.V. 16, 112. Built genome and transcriptome annotation database for Euglena gracilis using relational databases e.g. doi: 10.1002/1873-3468.12659, Tandon, P., Jin, Q., and Huang, L. (2017). 173, 4656. Identification and functional analysis of the geranylgeranyl pyrophosphate synthase gene (crtE) and phytoene synthase gene (crtB) for carotenoid biosynthesis in Euglena gracilis. Eng. Nevertheless, this study offered that lipid . doi: 10.1111/j.1529-8817.1986.tb00031.x, Kitaoka, M., Sasaki, T., and Taniguchi, H. (1993). However, there is no further information on whether this proposed system was ever built and tested. doi: 10.1016/j.mam.2007.01.002, Ritala, A., Hkkinen, S.T., Toivari, M., and Wiebe, M.G. Suzuki, K., Nakashima, A., Igarashi, M., Saito, K., Konno, M., Yamazaki, N., et al. Photosynthesis of Euglena gracilis under cobalamin-sufficient and -limited growing conditions. Large . doi: 10.2527/af.2013-0010, Lei, C., Ito, T., Ugawa, M., Nozawa, T., Iwata, O., Maki, M., et al. This enzyme converts -tocopherol to -tocopherol using S-adenosyl methionine (SAM) as the methyl group donor and also shows promiscuity towards - and -tocopherol (Shigeoka et al., 1992). Sci. E. gracilis has been a popular model organism and of considerable biotechnological interest, but the absence of a gene catalogue has hampered both basic research and translational efforts. Kuhaudomlarp, S., Patron, N.J., Henrissat, B., Rejzek, M., Saalbach, G., and Field, R.A. (2018). 57, 6369. Appl. J. doi: 10.1016/j.bej.2013.03.006, Choi, J.A., Oh, T.-H., Choi, J.-S., Chang, D.-J., and Joo, C.-K. (2013). (2017). Compared to some -tocopherol methyltransferases from plants, the E. gracilis enzyme has a high KM value (50 M for SAM) and low specific activity (251 nmol/h per mg protein for -tocopherol) (Shigeoka et al., 1992; Koch et al., 2003). Pharmaceut. (1963). Therefore, E. gracilis cell mass can be considered an excellent vitamin A supplement and could improve a vitamin A-poor diet. 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). Enhanced curdlan production in Agrobacterium sp. doi: 10.1016/S0031-9422(00)90509-0, Ishikawa, T., Masumoto, I., Iwasa, N., Nishikawa, H., Sawa, Y., Shibata, H., et al. Foods 46, 538545. 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: 10.1271/nogeikagaku1924.51.8_483, Innis, S.M. Arashida, R., and Mitra, S. (2015). Photoactivated adenylyl cyclase controls phototaxis in the flagellate Euglena gracilis. doi: 10.1124/jpet.105.085415, Richmond, A., Cheng-Wu, Z., and Zarmi, Y. Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: its unique molecular characterization. The mechanisms responsible for this observed reduction are still unclear, but may be related to an effect of paramylon on the gut microbiome (Watanabe et al., 2013). Phycologia 50, 156169. Nippon Nogeikagaku Kaishi 51, 483488. Trichoderma reesei, a superior cellulase source for industrial applications. (2014). (2018). U.S. Patent No 7.645,604. Scope of algae as third generation biofuels. Chem. Occurrence of L-ascorbic acid in Euglena gracilis Z. Microbiol. J. Chem. Braz. Homogeneous and heterogeneous environments were prepared, with only a red color or with a red circle surrounded by brighter white regions, respectively. Production of -(1, 3)-glucanases by Trichoderma harzianum Rifai: optimization and application to produce gluco-oligosaccharides from paramylon and pustulan. doi: 10.3945/an.114.006254, Tucci, S., Vacula, R., Krajcovic, J., Proksch, P., and Martin, W. (2010). Determination of the nutritive value of Euglena gracilis protein by in vitro digestion experiments and rat feeding tests. Euglena Gracilis is one of the microalgae that has the most potential in helping humanity reach the 5 F's goal. (2010). Euglena. Biomass Bioenergy 112, 138143. and their products currently on the market. Wax ester fermentation and its application for biofuel production, in Euglena: Biochemistry, Cell and Molecular Biology, eds S. D. Schwartzbach and S. Shigeoka (Cham: Springer International Publishing), 269283. (Table 1) (de Oliveira et al., 1999; Tokuoglu and nal, 2003; Ramazanov and Ramazanov, 2006;Rodrguez-Zavala et al., 2010). A key characteristic of E. gracilis are their two flagella, one of which is used for locomotion. So far, the highest reported total -tocopherol titres of 44.2 mg/L culture or 1.1 mg/g DW were achieved with E. gracilis in HT fed-batch cultivation after 455 h in a medium containing ethanol as a carbon source (Ogbonna et al., 1998). (2017). J. Phycol. doi: 10.1080/10408398.2016.1160362, Yadavalli, R., Rao, C.S., Rao, R.S., and Potumarthi, R. (2014). The study showed that Agrobacterium-mediated transformation was superior to electroporation and biolistic bombardment, resulting in stable E. gracilis transformants. Biotechnol. as a suitable source of lipids for potential use as biofuel and sustainable wastewater treatment. doi: 10.1016/j.carbpol.2018.08.005, Shibakami, M., Tsubouchi, G., and Hayashi, M. (2014). (2009). doi: 10.1111/jfd.12871, Yamamoto, F.Y., Yin, F., Rossi Jr, W., Hume, M., and Gatlin Iii, D.M. Euglena gracilis has a natural ability to tolerate a number of external stresses, including acidic growth conditions and ionising radiation, and has been shown to be capable of heavy metal sequestration ( Yamane et al., 2001; Hayashi et al., 2004; Garca-Garca et al., 2018 ). doi: 10.1292/jvms.71.885, Sumida, S., Ehara, T., Osafune, T., and Hase, E. (1987). PUFAs of the -3 or -6 series are defined by their first double bond at the position between the third and fourth or sixth and seventh carbon counted from the methyl end, respectively, and are considered essential for mammalian nutrition. doi: 10.3382/ps/pey227. The -carotene content of E. gracilis cell mass grown in this two-step cultivation process or under PT conditions (3.4 or 3.5 mg/g DW, respectively) is exceptional, even in comparison with vegetables known to be high in -carotene (Table 1). Biosynthesis of docosahexaenoic acid in Euglena gracilis: biochemical and molecular evidence for the involvement of a 4-fatty acyl group desaturase. Biotechnol. Lentinan with S-1 and paclitaxel for gastric cancer chemotherapy improve patient quality of life. Food Res. doi: 10.1007/s11095-018-2553-8, Shibakami, M., and Sohma, M. (2018). Shigeoka, S., Onishi, T., Nakano, Y., and Kitaoka, S. (1986). For example, intracellular lipids of a mutant strain generated by Fe-ion irradiation of the WT parental strain were stained with a boron-dipyrromethene dye (BODIPY505/515) to isolate high-producers using fluorescence-activated cell sorting. J. Clin. Delta-9 Elongases and Their Use in Making Polyunsaturated Fatty Acids. Yet, the influence of light was shown to be independent of the presence of chlorophyll, suggesting that mitochondria may be primarily responsible for the regulation of -tocopherol synthesis (Kusmic et al., 1998; Ogbonna et al., 1998; Fujita et al., 2008; Hasan et al., 2017). -1,3-glucan hydrolases from Euglena gracilis: II. (2015). Antioxidants 6, 118. doi: 10.1292/jvms.09-0526, Sugiyama, A., Suzuki, K., Mitra, S., Arashida, R., Yoshida, E., Nakano, R., et al. Buetow, D.E. Interactions between photoautotrophic and heterotrophic metabolism in photoheterotrophic cultures of Euglena gracilis. The nanofibres can be surface-modified with functional groups (e.g., carboxylic acid) and could serve as stimuli-responsive polymers or drug delivery systems (Shibakami et al., 2013b). 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). Homogeneous and heterogeneous environments were prepared, with only a red color or with a red circle surrounded by brighter white regions, respectively. Front. Sci. Algal Res. Eukaryot. J. -tocopherol, the major form of vitamin E in the US diet, deserves more attention. doi: 10.1006/abbi.1993.1383, Koch, M., Lemke, R., Heise, K.-P., and Mock, H.-P. (2003). Moreover, feeding male rats with 20 mg paramylon/kg BW daily was shown to improve the quality of their sperm (e.g., motility, vitality, and acrosome integrity) (Ak Sonat et al., 2018). Euglena live in fresh and brackish water habitats such as ponds rich in organic matter. US Department of Agriculture. 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). 56, 251258. J. Phycol. doi: 10.1128/ec.00097-06. Adv. J. Biol. Microbiol. doi: 10.1046/j.1432-1033.2003.03364.x, Koizumi, N., Sakagami, H., Utsumi, A., Fujinaga, S., Takeda, M., Asano, K., et al. Immunol. Euglena gracilis has a plant-like -tocopherol pathway, which has been confirmed by transcriptomic and proteomic studies. 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). Fish Shellfish Immunol. Plant Sci. 35, 5868. Recently, Khatiwada et al. The vicious cycle of vitamin a deficiency: a review. (2013). Alteration of wax ester content and composition in Euglena gracilis with gene silencing of 3-ketoacyl-coa thiolase isozymes. Euglena gracilis is a good source of vitamins A, C, and E and amino acids, which are essential for the human diet. Rev. Activation of macrophages by linear (1 3)--D-glucans. (2001). A promising approach to enhance microalgae productivity by exogenous supply of vitamins. Am. The flagellum they use for locomotion, which is slightly shorter than its body, beats by spinning at 40 Hz in close proximity to the cell body ().As for most flagellates, the swimming motion of E. gracilis is rototraslatory and inherently 3D. Figure 1. doi: 10.1007/s12257-010-0145-5, Zhu, G., Ou, Q., Zhang, T., Jiang, X., Sun, G., Zhang, N., et al. 21, 926936. 35, 5558. Biochemistry 2, 11481154. Phycol. Technol. The majority of the E. gracilis-derived lipids (WEs and FAs) are suitable for biodiesel production because they are saturated or have a low degree of unsaturation (Rosenberg, 1963; Tucci et al., 2010; Furuhashi et al., 2015). The methylerythritol phosphate pathway contributes to carotenoid but not phytol biosynthesis in Euglena gracilis. J. Appl. In an RNAi experiment, the latter enzyme has been shown to be essential for the ascorbate-dependent growth of the organism. (2015). Hydrolytic endo--1,3-glucanases: random cleavage of the polysaccharide chain (Takeda et al., 2015). (2018a). Shibakami, M., Shibata, K., Akashi, A., Onaka, N., Takezaki, J., Tsubouchi, G., et al. (2006). Biochim. Biochem. The lipid yield and the ratio of FAs/FAlcs to WEs have been shown to be strongly dependent on the cultivation conditions and the E. gracilis strain used (Tucci et al., 2010). BioSyst. Biotechnol. Algal Res. Chemistry, physico-chemistry and applications linked to biological activities of -glucans. (2003). Phytochemistry 116, 2127. Phycol. Fatty acyl-CoA reductase and wax synthase from Euglena gracilis in the biosynthesis of medium-chain wax esters. Levine, R.B., LeBrun, J.R., and Horst, G.P. Aghajanian, P., Hall, S., Wongworawat, M.D., and Mohan, S. (2015). !3 . Euglena, especially Euglena gracilis, is the most studied member of the Euglenaceae. (2018). Vitaminol. 2011; Sanghvi and Martin 2010 ). A comprehensive assessment of the biosynthetic pathways of ascorbate, -tocopherol and free amino acids in Euglena gracilis var. 343, 1018. doi: 10.1104/pp.103.034223, Ntefidou, M., Ldtke, T., Ahmad, M., and Hder, D.-P. (2006). 591, 13601370. doi: 10.1007/s00253-011-3311-6, Chae, S.R., Hwang, E.J., and Shin, H.S. Crit. environmental monitoring, divergent mechanisms for metabolic control, and novel . Aspects Med. 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). 30, 367373. FEBS Lett. In the Western world, major health conditions like cardiovascular and neurological diseases have been linked directly to a lack of long-chain -3 PUFAs, especially eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA), in the dietary intake (Deckelbaum and Torrejon, 2012; Innis, 2014). Biotechnol. Euglena gracilis shows an absolute requirement for vitamins B1 (thiamine) and B12 (cobalamin), so complex E. gracilis media usually contain at least 50 ng/L and 10 ng/L, respectively, of these compounds (Isegawa et al., 1987; Shigeoka et al., 1987; Croft et al., 2005; Hasan et al., 2017). WEs can be used directly as biodiesel, whereas FAs must be processed first by esterification with an alcohol to yield WEs. doi: 10.1111/jpy.12758, Sutivisedsak, N., Leathers, T.D., Bischoff, K.M., Nunnally, M.S., and Peterson, S.W. doi: 10.1016/0005-2744(67)90227-6, Matos, .P. A better understanding of the E. gracilis pathway for -carotene biosynthesis (Figure 2A) could hold the key to further improve the yields. Recent advances in our understanding of tocopherol biosynthesis in plants: an overview of key genes, functions, and breeding of vitamin E improved crops. 39, 4960. Prod. Mol. Suzuki, K. (2017). Exp. 29, 113. Biochem. Microalgae have been proposed as a source of feedstock for the production of biofuels such as biodiesel because of the high amounts of lipids, mostly FAs and WE, accumulated during the growth of some microalgal species (Matos, 2017). doi: 10.1371/journal.pone.0084871, Keywords: Euglena gracilis, biosynthesis, dietary protein, vitamins, polyunsaturated fatty acids, wax esters, paramylon, large-scale cultivation, Citation: Gissibl A, Sun A, Care A, Nevalainen H and Sunna A (2019) Bioproducts From Euglena gracilis: Synthesis and Applications. As a result, corneal epithelial cell migration was increased and the acute inflammatory reaction caused by corneal alkali burns in vivo was supressed (Choi et al., 2013). doi: 10.3389/fenrg.2016.00036, Andreani, L., and Rocha, J.D. These low titres could represent a good target for improvement by genetic engineering or non-recombinant metabolic engineering techniques based on the selection of improved phenotypes after the application of a selective pressure such as adaptive laboratory evolution (Portnoy et al., 2011; Dragosits and Mattanovich, 2013; Khatiwada et al., 2019). doi: 10.1186/s13068-015-0264-5, Ogawa, Y., Noda, K., Kimura, S., Kitaoka, M., and Wada, M. (2014). (2013). (2015). Paramylon also can act as a potent antioxidant protecting mice from acute hepatic injury induced by CCl4 treatment and was shown to alleviate non-alcoholic steatohepatitis in mice caused by a combination of streptozocin injection and high fat diet when orally administered at a dosage of 1 or 3 g/kg bodyweight (BW) per day, respectively (Sugiyama et al., 2009; Nakashima et al., 2018a). Amino Acids in Euglena gracilis Z. Microbiol gracilis cell mass can be considered an excellent vitamin a:... 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