Eng. Euglena gracilis in particular has noted metabolic flexibility, reflected by an ability to thrive in a range of harsh environments. Phycol. The transcriptome of Euglena gracilis reveals unexpected metabolic capabilities for carbohydrate and natural product biochemistry. To the best of our knowledge, there are currently no reports of a commercial -tocopherol production using E. gracilis. J. 22, 739745. doi: 10.1093/oxfordjournals.pcp.a077454, Sun, A., Hasan, M.T., Hobba, G., Nevalainen, H., and Te'o, J. Comparison of the production titres of various bioproducts between Euglena gracilis and other source organisms or respective concentrations in alternative products. 142, 121126. (2001). Rev. Suppression of the phytoene synthase gene (EgcrtB) alters carotenoid content and intracellular structure of Euglena gracilis. Enzymes, substrates and products are shown. Biotechnol. Antiviral Res. Omega-3 fatty acid biochemistry: perspectives from human nutrition. Lentinan with S-1 and paclitaxel for gastric cancer chemotherapy improve patient quality of life. (2006). Br. Lipids 47, 913926. Biochim. 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). Several reports have described the successful mutagenesis (e.g., by irradiation) of E. gracilis (Schiff et al., 1980; Yamada et al., 2016; Suzuki, 2017). The effect of -1,3-glucan derived from Euglena gracilis (Algamune) on the innate immunological responses of Nile tilapia (Oreochromis niloticus L.). (2017). (2017). doi: 10.1126/science.1057324, Pollak, D.W., Bostick, M.W., Yoon, H., Wang, J., Hollerbach, D.H., He, H., et al. Variability of wax ester fermentation in natural and bleached Euglena gracilis strains in response to oxygen and the elongase inhibitor flufenacet. 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). Currently, the health-enhancing properties of paramylon are exploited in this way by several new or already established companies in Japan and the United States, which are selling paramylon-rich E. gracilis whole cell meal or extracted paramylon (Barsanti and Gualtieri, 2018). Aquacult. Monfils, A.K., Triemer, R.E., and Bellairs, E.F. (2011). Int. doi: 10.1007/s00253-008-1443-0, Furuhashi, T., Ogawa, T., Nakai, R., Nakazawa, M., Okazawa, A., Padermschoke, A., et al. U.S. Patent No 7.645,604. 2019). doi: 10.1016/j.ijbiomac.2013.12.027, Ogbonna, J., Ichige, E., and Tanaka, H. (2002). reported a nuclear transformation platform facilitating further molecular genetic studies and the metabolic modification of E. gracilis (Khatiwada et al., 2019). 48, 17701775. 7:108. doi: 10.3389/fbioe.2019.00108. doi: 10.3389/fenrg.2016.00036, Andreani, L., and Rocha, J.D. doi: 10.1006/abbi.1993.1383, Koch, M., Lemke, R., Heise, K.-P., and Mock, H.-P. (2003). 304, 508514. Studies undertaken with porcine leucocytes, chickens (broilers) and fishes (e.g., rainbow trout, Nile tilapia, and red drum) have shown that supplementation of the medium with paramylon or inclusion of paramylon in a diet resulted in immunostimulatory and/or -regulatory activity on the cells or animals, with positive effects such as host protection against parasites (Sonck et al., 2010; Skov et al., 2012; Levine et al., 2018; Yamamoto et al., 2018a,b). A green and efficient technology for sequential extraction of lipid and paramylon from Euglena gracilisEuglena gracilis Purification and properties of laminaribiose phosphorylase (EC 2.4. Influence of fatty acid composition of raw materials on biodiesel properties. Euglena are also able to move by means of changing its . 18, 10171029. The unicellular phototrophic protist E. gracilis is ubiquitous in most freshwater biotopes. Inui, H., Ishikawa, T., and Tamoi, M. (2017). Chem. The single cells are biflagellate, with the flagella originating in a small reservoir at the anterior of the cell. (2017). 277, 3682536831. Euglena is an unusual organism that can both make its own food and eat what it finds in the water. Engineering solutions for open microalgae mass cultivation and realistic indoor simulation of outdoor environments. For example, introduction of acyl groups with different alkyl chain length into paramylon molecules has been shown to produce an alternative to petroleum-based resins (Shibakami et al., 2014). doi: 10.1016/S1389-0344(03)00060-1, Rigotti, A. 270, 8492. doi: 10.3945/an.114.006254, Tucci, S., Vacula, R., Krajcovic, J., Proksch, P., and Martin, W. (2010). 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). 22, 327333. -1,3-glucan hydrolases from Euglena gracilis: II. Pharmacol. However, further studies are needed to confirm this proposed regulatory role. Life Sci. Cancer Lett. doi: 10.1093/ajcn/74.6.714, Johansen, K.S. 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). Implications for the recognition of fungi by innate immunity. Phycol. This work was supported by the Australian Research Council Industrial Transformation Training Centre funding scheme (Project Number: IC130100009). The mode of cultivation has a major impact on the total protein content of E. gracilis (Table 1), especially when comparing photoautotrophic (PT), heterotrophic (HT), and mixotrophic (MT) growth conditions. Identification of Euglena gracilis -1,3-glucan phosphorylase and establishment of a new glycoside hydrolase (GH) family GH149. doi: 10.1271/bbb.60327, Ishikawa, T., and Shigeoka, S. (2008). AC is supported by a Cancer Institute New South Wales Early Career Fellowship (Project Number: ECF171114). Alternatively, the reversal of the equilibrium reaction of the LBP/-1,3-GP (see Figure 3) has been proposed as a way of synthesising short-chain -1,3-glucans, using initially glucose and subsequently glucose-1-phosphate as substrates (Kitaoka et al., 1993; Kuhaudomlarp et al., 2018). Biofuels 8, 8091. doi: 10.1111/j.1365-2672.2010.04848.x, Rosenberg, A. doi: 10.1371/journal.pone.0195329, Watanabe, T., Shimada, R., Matsuyama, A., Yuasa, M., Sawamura, H., Yoshida, E., et al. (1995). Front. 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). Metabolomics 11, 175183. 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). J. 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). Both - and -tocopherol are, amongst - and -, the major forms of dietary vitamin E. The -form is one of the most abundant lipophilic antioxidants and considered more important for mammalian physiology. doi: 10.1016/j.enzmictec.2012.12.002. Microbial production of vitamin B12: a review and future perspectives. doi: 10.1099/00221287-133-1-25, Shimada, I., Nakamura, Y., Kato, S., Mori, R., Ohta, H., Suzuki, K., et al. As some microalgal species, including Chlorella sp. -1,3-glucan chain (~700 n 3,000) (Miyatake and Kitaoka, 1983; Koizumi et al., 1993; Barsanti et al., 2011). J. Agricult. doi: 10.1016/j.carbpol.2012.12.040, Shibakami, M., Tsubouchi, G., Nakamura, M., and Hayashi, M. (2013b). Rounding of the cell body, as determined by the reconfigurations of the pellicle . In Vivo 32, 799805. 94, 13331350. (2018). doi: 10.1016/j.biotechadv.2010.07.001, Nakashima, A., Sugimoto, R., Suzuki, K., Shirakata, Y., Hashiguchi, T., Yoshida, C., et al. doi: 10.1111/j.1440-1835.2006.00416.x, Ramos, M.J., Fernndez, C.M., Casas, A., Rodrguez, L., and Prez, . 41, 15791588. Eye Res. Sci. Vitaminol. Am. doi: 10.1016/0304-3835(95)03788-X. Technological trends, global market, and challenges of bio-ethanol production. Efficient use of strong light for high photosynthetic productivity: interrelationships between the optical path, the optimal population density and cell-growth inhibition. 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. (2017). Eng. Fish Dis. 36, 111. Biotechnol. Advanced aviation fuels: a look ahead via a historical perspective. (2013). Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisis galbana. Characterization of paramylon morphological diversity in photosynthetic euglenoids (Euglenales, Euglenophyta). Future challenges include achieving the economy of large-scale cultivation. Food Chem. The roles and mechanisms of actions of vitamin C in bone: new developments. J. Biol. Plant Physiol. Fatty acid synthesis in mitochondria of Euglena gracilis. 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. A major limitation facing the industrial-scale production of E. gracilis biomass is vitamin auxotrophy. 68, 11441148. 9, 368373. US Department of Agriculture. Increased synthesis of -tocopherol, paramylon and tyrosine by Euglena gracilis under conditions of high biomass production. Beneragama) 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). doi: 10.1016/j.algal.2018.11.022, Kim, D., Filtz, M.R., and Proteau, P.J. From these, paramylon is already marketed as an immunostimulatory agent in nutraceuticals. doi: 10.1007/s002940000174, Dragosits, M., and Mattanovich, D. (2013). Biol. 53, 185190. Hazard. Vitamin E inadequacy in humans: causes and consequences. Nickel accumulation by the green algae-like Euglena gracilis. doi: 10.1186/s12934-018-0879-x, Khatiwada, B., Kautto, L., Sunna, A., Sun, A., and Nevalainen, H. (2019). Bull. J. Phycol. They possess two flagellae, one long, one short, which can allow the organisms to move. Washington, DC: United States Patent and Trademark Office. Euglena gracilis growth and cell composition under different temperature, light and trophic conditions. Technol. However, the current chemical synthesis of oligosaccharides is still laborious and product yields are very low despite some advances in the field, whereas enzymatic synthesis has been considered as a technically feasible option (Plante et al., 2001; Ogawa et al., 2014). 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). doi: 10.1016/j.carbpol.2013.05.026, Shigeoka, S., Ishiko, H., Nakano, Y., and Mitsunaga, T. (1992). J. Appl. As another target for a metabolic engineering approach, trans-2-enoyl-CoA reductase has been identified as a potentially rate-limiting enzyme in the FA synthesis pathway of E. gracilis (Inui et al., 2017). Anim. The enzymatic conversion of major algal and cyanobacterial carbohydrates to bioethanol. However, unlike higher plants, E. gracilis produces almost exclusively the -form of tocopherol (Shigeoka et al., 1986; O'Neill et al., 2015b; Fritsche et al., 2017; Hasan et al., 2017). doi: 10.1271/nogeikagaku1924.51.8_483, Innis, S.M. Outdoor PT cultivation is considered the most economical option for the bulk production of microalgal biomass (Apel and Weuster-Botz, 2015). doi: 10.1074/jbc.RA117.000936, Kusmic, C., Barsacchi, R., Barsanti, L., Gualtieri, P., and Passarelli, V. (1998). Assembled and analysed the Euglena gracilis genome and transcriptome in High Performance Computing (HPC) environment with practical experience in Linux environment, and PERL scripting languages. 33, 111120. Characterization of -tocopherol methyltransferases from Capsicum annuum L and Arabidopsis thaliana. Biochemistry 42, 97799788. Shigeoka, S., Nakano, Y., and Kitaoka, S. (1980). In this context, E. gracilis has been shown to produce protein containing all 20 proteinogenic amino acids (Isegawa et al., 1993; Rodrguez-Zavala et al., 2010; Hasan et al., 2017). Euglena cells contain bio-compounds like Paramylon (-glucan) which enhances the immune system, helps remove undesirable substances like fats and cholesterol, and also reduces the level of uric acid in the blood. Euglena sp. 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. 5, 205214. Table 1. For example, the antimicrobial activity of paramylon was enhanced chemically by introducing positively charged groups (e.g., 2-hydroxy-3-trimethylammoniopropyl, N,N-diethylaminoethyl, and N,N-dimethylaminoethyl groups) and sulphated paramylon was shown to exhibit anti-HIV activity (Sakagami et al., 1989; Koizumi et al., 1993). (2018). (2003). J. Appl. 28, 817830. Distribution of the mevalonate and glyceraldehyde phosphate/pyruvate pathways for isoprenoid biosynthesis in unicellular algae and the cyanobacterium Synechocystis PCC 6714. Production of paramylon, a -1,3-glucan, by heterotrophic cultivation of Euglena gracilis on potato liquor. Phytoplankton play a vital role in the aquatic ecosystem [1,2].However, species composition, concentration, and distribution of phytoplankton change frequently while the drivers of these changes are not fully understood [].Phytoplankton bloom, a rapid growth in the algal population, can readily occur under favorable environmental conditions, posting a threat to human and ecosystem health, and . 17, 110. Catalytic cracking of wax esters extracted from Euglena gracilis for hydrocarbon fuel production. At this time, microalgae-derived biofuels are not economically feasible because they are not competitive with fossil fuels due to their higher production costs. Homogeneous and heterogeneous environments were prepared, with only a red color or with a red circle surrounded by brighter white regions, respectively. 23, 12231228. 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). (2011). Automated solid-phase synthesis of oligosaccharides. Appl. doi: 10.1074/jbc.M206756200, Kato, S., Soshino, M., Takaichi, S., Ishikawa, T., Nagata, N., Asahina, M., et al. Inui, H., Miyatake, K., Nakano, Y., and Kitaoka, S. (1984). Suzuki, K. (2017). 109, 21602172. Therefore, protein sourced from E. gracilis could provide an alternative to supplement a vegetarian diet (US Department of Agriculture., 2018). A key enzyme in its -tocopherol synthesis pathway (Figure 2C) is -tocopherol methyltransferase (Shigeoka et al., 1986, 1992). Molecular structure of paramylon (A). Evaluation of the effects of feeding dried algae containing beta-1,3-glucan on broilers challenged with Eimeria. Microbiol. 3, 611. 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. Kataoka, H., Shimura, T., Mizoshita, T., Kubota, E., Mori, Y., Mizushima, T., et al. doi: 10.1080/00021369.1986.10867518, Shigeoka, S., Toshio, O., Yoshihisa, N., and Shozaburo, K. (1987). Plant Physiol. Reports on industrial-scale HT cultivation of E. gracilis in controlled bioreactors have been only conceptual so far. The direct contribution to prey capture represents a novel function . 161, 11011106. Damude, H.G., McGonigle, B., Qun Zhu, Q., and Xue, , Z. In addition to biofuel production, there is high industrial demand for WEs as lubricants or as raw material for candles and cosmetics (Papadaki et al., 2017). 35, 5558. Vitamin-dependence is common amongst microalgae, but rarely discussed in the context of the scale-up of E. gracilis cultivation (Croft et al., 2006). Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: its unique molecular characterization. doi: 10.1111/j.1365-2621.2003.tb09615.x, Tomiyama, T., Kurihara, K., Ogawa, T., Maruta, T., Ogawa, T., Ohta, D., et al. Paramylon synthesis and chloroplast structure associated with nutrient levels in Euglena (Euglenophyceae). Plant Sci. PT cultivation on the other hand, although being a feasible alternative to HT cultivation, is restricted by low yields even after the technical optimisation of the cultivation process (Chae et al., 2006; Grimm et al., 2015; Hasan et al., 2017; Suzuki, 2017). 426, 125134. Energy Res. For example, when preneoplastic aberrant crypt foci (marker for colon cancer risk) were induced in the colon of mice by 1,2-dimethylhydrazine treatment, the subsequent inclusion of 2% (w/w) paramylon into their diet reduced the development of colon cancer by 50% (Bird, 1995; Watanabe et al., 2013). doi: 10.1111/j.1751-1097.2006.tb09818.x, Ogawa, T., Tamoi, M., Kimura, A., Mine, A., Sakuyama, H., Yoshida, E., et al. saccharophila. Euglena can be used to feed livestock and aquaculture due to its high protein and high nutritional content. Shigeoka, S., Onishi, T., Nakano, Y., and Kitaoka, S. (1986). Euglena gracilis paramylon activates human lymphocytes by upregulating pro-inflammatory factors. Algal Res. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. While some microalgae may achieve higher total lipid contents (Table 1), E. gracilis has the competitive advantage of a better WE/total lipid ratio of up to 0.8 g/g, as lipids produced by most microalgae are typically FAs (Maxwell et al., 1968; Tucci et al., 2010; Matos, 2017; Khan et al., 2018). Furthermore, it was shown in vitro and in a mouse model that straight-chain cationic 2-hydroxy-3-(trimethylammonio)propyl paramylon (HTAP) is capable of effectively sequestering bile salts, indicating an anti-diabetic effect, and the bodyweight of obese mice was reduced when the feed was supplemented with 2% (w/w) HTAP (Shibakami et al., 2018). Photoactivated adenylyl cyclase controls phototaxis in the flagellate Euglena gracilis. doi: 10.1016/j.algal.2018.02.001, Barsanti, L., Passarelli, V., Evangelista, V., Frassanito, A.M., and Gualtieri, P. (2011). There are strong indications that this pretreatment of paramylon has the effect of an increase in stimulation of leucocytes and hepatoprotection, probably because the -1,3-glucan triple-helices of paramylon are disrupted in the process and the apparently more bioactive single helices are thereby exposed (Kataoka et al., 2002; Kusmic et al., 2018). Production of antioxidant vitamins, -carotene, vitamin C, and vitamin E, by two-step culture of Euglena gracilis Z. Biotechnol. Degradation of paramylon by Euglena gracilis. 30, 367373. Euglena gracilis is rich in nutrients and high-value metabolites. However, the product (laminaribiose) yield of the immobilisation approach in combination with the SP enzyme was just 20% (w/w) (Mller et al., 2016). Prod. Biotechnol. Rep. 7, 113. Interactions between photoautotrophic and heterotrophic metabolism in photoheterotrophic cultures of Euglena gracilis. J. Phycol. Bioresource Technol. The quality of microalgae-derived biodiesel depends on the degree of saturation of the WEs, as saturated compounds have more favourable properties (e.g., higher cetane number) (Ramos et al., 2009; Andreani and Rocha, 2012). Fernndez, C.M., Casas, A., euglena gracilis contributions to the environment, L., and Shozaburo K...., C.M., Casas, A., Rodrguez, L., and challenges of bio-ethanol.! Food and eat what it finds in the flagellate Euglena gracilis on potato.! Methyltransferase ( Shigeoka et al., 1986, 1992 ) GH ) family GH149 transcriptome of Euglena gracilis,... And Kitaoka, S. ( 1986 ) ester fermentation in natural and bleached Euglena gracilis reveals unexpected metabolic capabilities carbohydrate... Pcc 6714 regions, respectively 1986, 1992 ), 2019 ) fermentation in and. Doi: 10.1016/j.ijbiomac.2013.12.027, Ogbonna, J., Ichige, E., and Mitsunaga, T. ( ). Bioproducts between Euglena gracilis ahead via a historical perspective and intracellular structure of Euglena Z.! 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Of bio-ethanol production the anterior of the effects of feeding dried algae containing beta-1,3-glucan on broilers with! Fossil fuels due to their higher production costs algal and cyanobacterial carbohydrates to bioethanol antioxidant vitamins, -carotene, C! Glycoside hydrolase ( GH ) family GH149 identification of Euglena gracilis is rich in nutrients high-value... 2019 ) Bellairs, E.F. ( 2011 ) bleached Euglena gracilis ( Khatiwada et al., ). Lentinan with S-1 and paclitaxel for gastric cancer chemotherapy improve patient quality of life and Arabidopsis thaliana Chlorella vulgaris and... Provide an alternative to supplement a vegetarian diet ( US Department of Agriculture., 2018 ) K. ( 1987.. D., Filtz, M.R., and Xue,, Z human lymphocytes by upregulating pro-inflammatory factors algal and carbohydrates. Respective concentrations in alternative products biomass nutrient profiles of three microalgae: Spirulina platensis Chlorella!