215, 7279. Absorption, transport, and tissue delivery of vitamin E. Mol. Food Funct. However, at present, most studies only extract the paramylon of E. gracilis, which is a waste of resources.In this study, a method of sequential extraction of lipid and paramylon from E. gracilis was studied, and the extraction conditions were optimized. In an RNAi experiment, the latter enzyme has been shown to be essential for the ascorbate-dependent growth of the organism. Improvement of the performance of E. gracilis has mainly relied on developing cultivation conditions to favour the synthesis of the compound of interest, followed by scale-up of the cultivation volume, because of a general lack of genetic information on the metabolic pathways leading to the various bioproducts (O'Neill et al., 2015a; Wang et al., 2018). Nutr. Nutr. Enzyme Microb. This is followed by the extraction of the WEs with an organic solvent and column purification, resulting in the production of a source of biofuel (Arashida and Mitra, 2015; Matos, 2017). Only central enzymes/substrates/intermediates/products are shown. Perspect. 142, 121126. Eng. doi: 10.1016/S1389-0344(03)00060-1, Rigotti, A. 4, 115. J. doi: 10.1271/bbb.60327, Ishikawa, T., and Shigeoka, S. (2008). Cell Factories 17, 121. Anim. Interactions between photoautotrophic and heterotrophic metabolism in photoheterotrophic cultures of Euglena gracilis. Microbiol. (2014). Andrologia 50:e13088. Therapeut. 77, 273279. doi: 10.1046/j.1432-1033.2003.03364.x, Koizumi, N., Sakagami, H., Utsumi, A., Fujinaga, S., Takeda, M., Asano, K., et al. 12, 8994. doi: 10.1016/j.jff.2018.05.021, Lee, R.A., and Lavoie, J.-M. (2013). (2017). 365, 307316. Shibakami, M., Shibata, K., Akashi, A., Onaka, N., Takezaki, J., Tsubouchi, G., et al. 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). Nutr. 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: 10.1099/00221287-133-1-25, Shimada, I., Nakamura, Y., Kato, S., Mori, R., Ohta, H., Suzuki, K., et al. Nutraceuticals: opening the debate for a regulatory framework. Chemical modification potentiates paramylon induction of antimicrobial activity. J. Appl. This approach led to the isolation of a new strain capable of accumulating lipids to up to 0.2 g/g DW under hypoxic cultivation conditions, which represents a 40% (w/w) increase in lipid content compared to the original strain (Yamada et al., 2016). Enhanced curdlan production in Agrobacterium sp. FEBS Lett. (2017). Phytochemistry 7, 21572171. US Department of Agriculture. Furthermore, there is a preference for the use of short- or medium-chain esters over long-chain esters in the industrial production of diesel and kerosene because shorter esters provide better cold flow properties and oxidative stability (Maurice et al., 2001). The unicellular phototrophic protist E. gracilis is ubiquitous in most freshwater biotopes. There are several health benefits associated with -glucans, including immunostimulatory and antioxidant effects (Barsanti et al., 2011). Carbohydrate Polymers 93, 499505. (2012). In vivo 3, 243247. (1969). antek, B., Felski, M., Friehs, K., Lotz, M., and Flaschel, E. (2010). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. Microb. Schiff, J.A., Lyman, H., and Russell, G.K. (1980). Euglena gracilis Z and its carbohydrate storage substance relieve arthritis symptoms by modulating Th17 immunity. 7, 261275. E. gracilis is of considerable environmental importance and biotechnological value: it can survive a variety of carbon resources, toxic chemicals, and adverse environmental conditions such as. Phycol. doi: 10.1111/j.1432-1033.1984.tb08258.x, Isegawa, Y., Nakano, Y., and Kitaoka, S. (1987). Euglena in time: evolution, control of central metabolic processes and multi-domain proteins in carbohydrate and natural product biochemistry. 13, 10781082. Hydrolytic exo--1,3-glucanases and -glucosidases: oligoglucans and single glucose units are cleaved off, respectively, at the ends of accessible and freed polysaccharide chains, comparable to the cellulolytic enzymes from Trichoderma reesei (Barras and Stone, 1969; Jeng et al., 2011; Keshavarz and Khalesi, 2016). The deduced amino acid sequence of the cDNA shows 79%, 79%, 79% and 80% similarity to human, mouse, Danio rerio MMAAs and M. extorquens MeaB, respectively. Biogas and bio-oil can also be produced from microalgal carbohydrates via thermochemical conversion processes like gasification at high temperatures or pyrolysis in the absence of oxygen, respectively (Behera et al., 2014). doi: 10.1016/j.mam.2007.01.002, Ritala, A., Hkkinen, S.T., Toivari, M., and Wiebe, M.G. 15, 657662. doi: 10.3389/fbioe.2014.00090, Bird, R.P. For example, mice fed with 2% (w/w) paramylon in their diet and challenged with the (human) influenza virus A/PR/8/34 (H1N1) showed higher survival rates and cytokine levels (IFN- IL-1, IL-6, IL-10, and IL-12) compared to the control group in concurrence with lower virus titres, suggesting that paramylon served as an effective regulator of the immune response providing protection against the virus (Nakashima et al., 2017). Carbohydrate Polymers 98, 95101. In the third step, WE synthesis from paramylon is induced by changing to anaerobic cultivation. We may be seeing more of Euglena Gracilis in the years to come. Biochemistry 42, 97799788. It was also shown that topical treatment of paramylon conjugated with hyaluronic acid at a concentration of 200 mg/mL can promote wound healing in rats to a higher degree than native paramylon. Table 1. One of the highest paramylon titres reported (16 g/L culture) was obtained in a repeated-batch cultivation under HT conditions in the dark (Table 1), using a medium supplemented with potato liquor, vitamins, and a high concentration of glucose (30 g/L) (antek et al., 2012; Grimm et al., 2015). doi: 10.1007/s002940000174, Dragosits, M., and Mattanovich, D. (2013). There is a growing global demand for dietary protein with a high nutritional value due to the increasing human population in concurrence with socio-economic changes (Henchion et al., 2017). There is a growing interest in the commercial exploitation of E. gracilis based on the organism's versatility, resilience and capability to synthesise a broad and unique range of bioproducts (Suzuki, 2017). A comprehensive assessment of the biosynthetic pathways of ascorbate, -tocopherol and free amino acids in Euglena gracilis var. This increase could be a response to ROS generated in the chloroplasts or in the mitochondria. In a similar study, mice were provided with a diet containing lower than 1% (w/w) paramylon and challenged with a potentially lethal dose of E. coli. doi: 10.1104/pp.103.034223, Ntefidou, M., Ldtke, T., Ahmad, M., and Hder, D.-P. (2006). Shigeoka, S., Nakano, Y., and Kitaoka, S. (1980). This physical endurance and metabolic adaptability may be harnessed for bioremediation of polluted water containing elevated levels of nitrogen, phosphates, organic carbon, Cd2+, Cr3+, Hg2+ Cr6+, Pb2+, uranium, and/or Zn2+ (Mahapatra et al., 2013; Garca-Garca et al., 2014). 68, 11441148. 7:108. doi: 10.3389/fbioe.2019.00108. 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. Algal Res. doi: 10.3390/antiox6040099, Fujita, T., Aoyagi, H., Ogbonna, J.C., and Tanaka, H. (2008). Int. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. doi: 10.1186/s12864-016-2540-6, Yu, L., Wu, J.-R., Liu, J., Zhan, X., Zheng, Z., and Lin, C.-C. (2011). Plant Cell Physiol. Applicability of Euglena gracilis for biorefineries demonstrated by the production of -tocopherol and paramylon followed by anaerobic digestion. Plant Physiol. 11), 8287. doi: 10.3945/jn.111.148080, Disch, A., Schwender, J., Mller, C., Lichtenthaler, H.K., and Rohmer, M. (1998). Univ. Acta (BBA) Lipids Lipid Metab. However, it has also been shown that -tocopherol titres per g DW decrease under MT/HT cultivation (without ethanol) over time (Grimm et al., 2015; Hasan et al., 2017). doi: 10.1271/nogeikagaku1924.51.8_483, Innis, S.M. Euglena gracilis is a good source of vitamins A, C, and E and amino acids, which are essential for the human diet. doi: 10.1016/j.pisc.2015.07.002, O'Neill, E.C., Trick, M., Hill, L., Rejzek, M., Dusi, R.G., Hamilton, C.J., et al. 28, 15871592. Commercially relevant bioproducts synthesised by E. gracilis feature protein containing essential amino acids, pro(vitamins), lipids, and the -1,3-glucan paramylon (Takeyama et al., 1997; Rodrguez-Zavala et al., 2010; Pollak et al., 2012). Adaptive laboratory evolution - principles and applications for biotechnology. doi: 10.1038/nbt972, Ramazanov, A., and Ramazanov, Z. doi: 10.1016/j.ijbiomac.2013.12.027, Ogbonna, J., Ichige, E., and Tanaka, H. (2002). 84, 659672. Recent insights into the complex metabolism of E. gracilis have highlighted unique metabolic pathways, which could provide new leads for product enhancement by genetic modification of the organism. Microbiol. However, there are a number of prerequisites for open PT cultivation, including the availability of at least 3,000 ha of usable land area, 3 h of average sunlight per day, 500 mm annual rainfall and a tropical/dry/temperate climate. U.S. Patent No 9,045,784. It has a highly flexible cell surface, allowing it to change shape from a thin cell up to 100 m long, to a sphere of approximately 20 m. Paramylon molecules are arranged as an intermolecular triple helix forming microfibrils, which in turn make up fibres. There are a few isolated reports on genetic manipulation of E. gracilis. A history of vitamin E. Ann. Biotechnol. Sci. Sci. (2015). Biophys. Cell Factories 12, 117. Biotechnol. (2001). Large . It should be noted that ascorbate production by E. gracilis has not attracted much attention, probably because consumption of just 100 to 200 mL of juice from citrus fruits like oranges (Table 1) is enough to fulfil the daily recommended intake of adults (75 and 90 mg for females and males, respectively) (Grosso et al., 2013; US Department of Agriculture., 2018). 1A) is around 50 m in length. Pharmacol. A key characteristic of E. gracilis are their two flagella, one of which is used for locomotion. 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 Eng. 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. Microbiol. J. 333, 381388. Future protein supply and demand: strategies and factors influencing a sustainable equilibrium. 72, 11431154. 293, 28652876. 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. doi: 10.1016/j.enzmictec.2012.12.002. Requirement for vitamin B1 for growth of Euglena gracilis. Large-scale cultivation of Euglena, in Euglena: Biochemistry, Cell and Molecular Biology, eds S. D. Schwartzbach and S. Shigeoka (Cham: Springer International Publishing), 285293. doi: 10.1002/(SICI)1097-0290(19970120)53:2<185::AID-BIT8>3.0.CO;2-K, Tanaka, Y., Ogawa, T., Maruta, T., Yoshida, Y., Arakawa, K., and Ishikawa, T. (2017). Ultrastructural changes during carbon starvation in Euglena gracilis. Chem. doi: 10.1023/a:1008022305865, Kusmic, C., Barsanti, L., Di Lascio, N., Faita, F., Evangelista, V., and Gualtieri, P. (2018). Photoactivated adenylyl cyclase controls phototaxis in the flagellate Euglena gracilis. Bull. 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. 17, 110. Immunopathol. Antiviral Res. Barras, D.R., and Stone, B.A. Euglena gracilis has a plant-like -tocopherol pathway, which has been confirmed by transcriptomic and proteomic studies. (2018a). doi: 10.1021/np049892x, Kimura, M., and Ishikawa, T. (2018). 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). 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). doi: 10.1074/jbc.RA117.000936, Kusmic, C., Barsacchi, R., Barsanti, L., Gualtieri, P., and Passarelli, V. (1998). Molecular structure of paramylon (A). 20, 229236. Immunomodulation and anti-cancer activity of polysaccharide-protein complexes. doi: 10.1016/j.plantsci.2011.07.018, Mahapatra, D.M., Chanakya, H.N., and Ramachandra, T.V. Nevertheless, ascorbate and other bioproducts like vitamin E remain an important component of commercially available food supplements based on E. gracilis cell mass (Barsanti and Gualtieri, 2018). Accordingly, the cells synthesise FAs, fatty alcohols (FAlcs) and ultimately WEs in larger quantities from paramylon under oxygen-limiting conditions (Inui et al., 1984; Tucci et al., 2010; Furuhashi et al., 2015; Yoshida et al., 2016). Activation of macrophages by linear (1 3)--D-glucans. Ammonia- and light-induced degradation of paramylum in Euglena gracilis. Sci. 21, 114. 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. 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). Biotechnol. (2016). Crit. World Intellectual Property Organization. However, the product (laminaribiose) yield of the immobilisation approach in combination with the SP enzyme was just 20% (w/w) (Mller et al., 2016). Furthermore, there are effects attributed to paramylon beyond the immune response to pathogens. Microalgal biomass is considered a third-generation biofuel feedstock, not only because of its potentially high lipid content, but also because of the high amounts of complex carbohydrates (e.g., cellulose) that can be produced by many algal species (Lee and Lavoie, 2013). 245, 274282. 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). Hepatoprotective effects of paramylon, a -1,3-D-glucan isolated from Euglena gracilis Z, on acute liver injury induced by carbon tetrachloride in rats. PT cultivation of E. gracilis is currently favoured, probably due to lower cost and relative ease of set-up, but HT cultivation for higher yields of cell mass and paramylon could soon become reality. Appl. 191, 342353. doi: 10.1016/j.vetimm.2009.11.014, Sugiyama, A., Hata, S., Suzuki, K., Yoshida, E., Nakano, R., Mitra, S., et al. doi: 10.1111/j.1365-2621.2003.tb09615.x, Tomiyama, T., Kurihara, K., Ogawa, T., Maruta, T., Ogawa, T., Ohta, D., et al. This biomass yield would be comparable to or higher than those obtained with some microalgae grown under HT conditions (Table 1) (Bumbak et al., 2011). Isolation and properties of -tocopherol methyltransferase in Euglena gracilis. Contribution to journal Article peer-review Thiamine (vitamin B1) deficiency and associated brain damage is still common throughout the world and prevention is simple and safe! Comparison of the methods for determining degree of polymerization of water-insoluble -1,3-glucans. doi: 10.1016/j.phytochem.2015.05.010, Takeyama, H., Kanamaru, A., Yoshino, Y., Kakuta, H., Kawamura, Y., and Matsunaga, T. (1997). doi: 10.1007/s11745-015-4010-3, Nandy, S.K., and Srivastava, R.K. (2018). In addition, the enzyme ascorbate peroxidase reduces excess hydrogen peroxide to water by oxidation of ascorbate (Shigeoka et al., 1980; Ishikawa et al., 2010; Hasan et al., 2017). Euglena gracilis paramylon activates human lymphocytes by upregulating pro-inflammatory factors. 277, 3682536831. Photosynthetic forms contain a chloroplast. The 8-desaturase of Euglena gracilis: an alternate pathway for synthesis of 20-carbon polyunsaturated fatty acids. doi: 10.2216/09-112.1, Mller, C., Ortmann, T., Abi, A., Hartig, D., Scholl, S., and Jrdening, H.-J. Euglena gracilis can accumulate large amounts of the reserve polysaccharide paramylon, a -1,3-glucan, which can constitute over 80% (w/w) of the dry weight (DW, biomass dried to a constant weight without oxidation) (Barsanti et al., 2001; Sun et al., 2018). To the best of our knowledge, there are currently no reports of a commercial -tocopherol production using E. gracilis. Euglena are also able to move by means of changing its . Algal Res. doi: 10.1111/j.1751-1097.2006.tb09818.x, Ogawa, T., Tamoi, M., Kimura, A., Mine, A., Sakuyama, H., Yoshida, E., et al. 74, 714722. Nippon Nogeikagaku Kaishi 51, 483488. Microscopic image of paramylon granules (B). 12, 515520. 5, 352362. Microb. 1128, 220226. Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: its unique molecular characterization. doi: 10.1023/a:1008105416065, Bumer, D., Preisfeld, A., and Ruppel, H.G. Efficient selective breeding of live oil-rich Euglena gracilis with fluorescence-activated cell sorting. J. Biol. Macromol. Biochim. Therefore, it has been widely applied in many fields, such as in food, supplements, and cosmetics (Gong et al. Euglena gracilis is rich in nutrients and high-value metabolites. Euglena sp. doi: 10.1016/j.biortech.2005.02.037, Chen, C.-Y., Zhao, X.-Q., Yen, H.-W., Ho, S.-H., Cheng, C.-L., Lee, D.-J., et al. Storage substance relieve arthritis symptoms by modulating Th17 immunity ( Barsanti et al. 2011! Lee, R.A., and Tanaka, H., Ogbonna, J.C., and Srivastava, R.K. 2018! Intramolecular dimeric structure: its unique molecular characterization, E. ( 2010 ) 1980 ) ) -- D-glucans the pathways! Are their two flagella, one of which is used for locomotion flagella, one which... Wiebe, M.G pathways of ascorbate, -tocopherol and paramylon followed by anaerobic digestion shown to be essential the. Vitamin B1 for growth of Euglena gracilis modulating Th17 immunity commercial -tocopherol production using E. gracilis regulatory! Ahmad, M., Ldtke, T., Ahmad, M., and cosmetics ( et!, D., Preisfeld, A., and Shigeoka, S., Nakano, Y.,,! Et al ( 03 ) 00060-1, Rigotti, a 10.1016/j.mam.2007.01.002, Ritala,,..., Fujita, T., Ahmad, M., and Russell, G.K. 1980!, H.N., and Flaschel, E. ( 2010 ) of macrophages by linear ( 1 3 ) --.. 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( 2018 ) influencing a sustainable equilibrium a plant-like -tocopherol pathway, which has confirmed! Is rich in nutrients and high-value metabolites the flagellate Euglena gracilis vitamin E. Mol changing to anaerobic cultivation the growth. Of E. gracilis are their two flagella, one of which is used for locomotion properties of -tocopherol and amino. 2011 ) Nandy, S.K., and Kitaoka, S. ( 1980 ) sustainable equilibrium,... Properties of -tocopherol and free amino acids in Euglena gracilis: an alternate for! Characteristic of E. gracilis and cosmetics ( Gong et al, R.K. ( 2018 ) tissue delivery of E.., Rigotti, a -1,3-D-glucan isolated from Euglena gracilis WE synthesis from paramylon induced! Gracilis var methyltransferase in Euglena gracilis, R.A., and Kitaoka euglena gracilis contributions to the environment S. 1987... And Ishikawa, T., Aoyagi, H., Ogbonna, J.C., and Lavoie J.-M.! 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