(2018). Homogeneous and heterogeneous environments were prepared, with only a red color or with a red circle surrounded by brighter white regions, respectively. A better understanding of the E. gracilis pathway for -carotene biosynthesis (Figure 2A) could hold the key to further improve the yields. 52, 203210. doi: 10.1186/s12870-017-1066-7, Kato, S., Takaichi, S., Ishikawa, T., Asahina, M., Takahashi, S., and Shinomura, T. (2016). A green and efficient technology for sequential extraction of lipid and paramylon from Euglena gracilisEuglena gracilis Biofuels 8, 8091. (2018). Single-cell analysis of morphological and metabolic heterogeneity in Euglena gracilis by fluorescence-imaging flow cytometry. J. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). Euglena. Poultry Sci. Paramylon (-1,3-glucan) content in wild type and WZSL mutant of Euglena gracilis. doi: 10.3389/fbioe.2014.00090, Bird, R.P. PT cultivation induces the synthesis of ascorbate in E. gracilis as a mechanism to cope with reactive oxygen species (ROS) produced during photosynthesis (ROS scavenging). Therefore, paramylon may be a suppressant of the T helper cells (Th) type 1 and type 2 responses and could be used as a potential therapy for AD (Sugiyama et al., 2010). Biochem. 142, 121126. Euglena gracilis biosynthesis pathways of -carotene (A), ascorbate (B), -tocopherol (C), and polyunsaturated fatty acids (D) (Shigeoka et al., 1992; Kim et al., 2004; Ishikawa et al., 2006; Ishikawa and Shigeoka, 2008; Lohr et al., 2012; Pollak et al., 2012; O'Neill et al., 2015b; Kato et al., 2016; Hasan et al., 2017). Br. 20, 229236. Advertisement randellpierre23 Answer: doi: 10.1002/apj.1805, Yamada, K., Suzuki, H., Takeuchi, T., Kazama, Y., Mitra, S., Abe, T., et al. Paramylon is uniquely produced by euglenoids, deposited as granules in the cytosol, and readily degraded and utilised as a carbon source under carbon starvation (Malkoff and Buetow, 1964; Kiss et al., 1986; Barsanti et al., 2001; Monfils et al., 2011). Importantly, animal and in vitro studies have shown an excellent digestibility of protein derived from E. gracilis biomass (Hosotani and Kitaoka, 1977). 35, 5868. J. Appl. Microb. Multi-stage Process for Production of Immune Modulator. The cell motion of Euglena gracilis in homogeneous and heterogeneous light environments was analyzed. 11), 8287. 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). 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. 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). Unlocking the biological potential of Euglena gracilis: evolution, cell biology and significance to parasitism. Soc. Use of ionic liquids in biodiesel production: a review. 31, 107115. Biochem. In Vivo 32, 799805. 333, 381388. doi: 10.1039/C3MT00313B, Garca-Garca, J.D., Pea-Sanabria, K.A., Snchez-Thomas, R., and Moreno-Snchez, R. (2018). Sci. doi: 10.1039/C3FO60256G, Weber, D., and Grune, T. (2012). Recent advances in our understanding of tocopherol biosynthesis in plants: an overview of key genes, functions, and breeding of vitamin E improved crops. 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). Biomed. Regardless of the cultivation mode, dried E. gracilis cell mass would be competitive in terms of its protein content with fresh high-protein animal products such as beef, chicken or fish, of which the protein content usually does not exceed 0.4 g/g after cooking (Table 1). Eur. J. Phycol. However, DW titres of E. gracilis under PT conditions are significantly lower than those obtained with MT/HT growth (Table 1) (Takeyama et al., 1997; Hasan et al., 2017). (2001). doi: 10.1186/s13068-015-0264-5, Ogawa, Y., Noda, K., Kimura, S., Kitaoka, M., and Wada, M. (2014). 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. 270, 8492. Consequently, -carotene titres per g DW are highest under PT cultivation conditions (Table 1). -glucan in foods and its physiological functions. J. Struct. (2010). In this study, we examined the effect of paramylon intake on the circadian clock. doi: 10.1590/S0104-66322012000100001, Apel, A.C., and Weuster-Botz, D. (2015). 58, 15041505. (2005). Chemistry, physico-chemistry and applications linked to biological activities of -glucans. Thermal, crystalline, and pressure-sensitive adhesive properties of paramylon monoesters derived from an euglenoid polysaccharide. doi: 10.1016/0166-3542(93)90063-O. doi: 10.1364/BOE.7.002703, Levine, R., Horst, G., Tonda, R., Lumpkins, B., and Mathis, G. (2018). Eng. Pharmacol. Production of paramylon, a -1,3-glucan, by heterotrophic cultivation of Euglena gracilis on potato liquor. A key enzyme in its -tocopherol synthesis pathway (Figure 2C) is -tocopherol methyltransferase (Shigeoka et al., 1986, 1992). 38, 9951008. (2014). Relative metal toxicities were evaluated based on the Effective Exposure causing 50% growth reduction (= EE50). Inui, H., Miyatake, K., Nakano, Y., and Kitaoka, S. (1984). (2010). Comparative studies between laminaribiose- and -1,3-oligoglucan phosphorylase. (2013). (2013). doi: 10.1016/0005-2744(69)90253-8, Barsanti, L., Bastianini, A., Passarelli, V., Tredici, M.R., and Gualtieri, P. (2000). 70, 27202726. Biochemistry 2, 11481154. Eng. Phytochemistry 7, 21572171. Bull. Whereas 3D tracking of swimming microorganisms is a long-standing . doi: 10.1016/j.biombioe.2018.03.004, Skov, J., Kania, P.W., Holten-Andersen, L., Fouz, B., and Buchmann, K. (2012). 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). Univ. 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). US Department of Agriculture. (2017). Bioprocess Biosyst. High-throughput label-free image cytometry and image-based classification of live Euglena gracilis. The 8-desaturase of Euglena gracilis: an alternate pathway for synthesis of 20-carbon polyunsaturated fatty acids. Comparison of the production titres of various bioproducts between Euglena gracilis and other source organisms or respective concentrations in alternative products. Food Sci. Interactions between photoautotrophic and heterotrophic metabolism in photoheterotrophic cultures of Euglena gracilis. (2016). 8, 118. Cell Factories 16, 113. Antitumor activity of the -glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice. Abstract Motile microorganisms such as the green Euglena gracilis use a number of external stimuli to orient in their environment. (1967). 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. Several reports have described the successful mutagenesis (e.g., by irradiation) of E. gracilis (Schiff et al., 1980; Yamada et al., 2016; Suzuki, 2017). Many of the last enzymatic steps between the central intermediate isopentenyl pyrophosphate and the end product remain to be elucidated, as only the enzymes geranylgeranyl pyrophosphate synthase and phytoene synthase (see Figure 2A) have been verified by complementing the partially deleted carotenoid biosynthetic pathway of Pantoea ananatis expressed in E. coli with E. gracilis enzymes (Kato et al., 2016). Eng. Biochem. At present, only two enzymes of this pathway, the D-galacturonate reductase and aldonolactonase, have been biochemically characterised in vitro. doi: 10.3177/jnsv.64.8, Nakazawa, M., Andoh, H., Koyama, K., Watanabe, Y., Nakai, T., Ueda, M., et al. doi: 10.3945/an.114.006254, Tucci, S., Vacula, R., Krajcovic, J., Proksch, P., and Martin, W. (2010). Inui, H., Ishikawa, T., and Tamoi, M. (2017). Quantitative study on lipid productivity of Euglena gracilis and its biodiesel production according to the cultivation conditions . 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). Kataoka, K., Muta, T., Yamazaki, S., and Takeshige, K. (2002). Delta-9 Elongases and Their Use in Making Polyunsaturated Fatty Acids. Large scale cultivation of genetically modified microalgae: a new era for environmental risk assessment. Res. The effects of dietary restriction and administration of -glucan from Euglena gracilis on the sperm characteristics and reproductive organs of rats. Microscopic image of paramylon granules (B). *Correspondence: Anwar Sunna, anwar.sunna@mq.edu.au, Creative Commons Attribution License (CC BY). Also, it has been suggested to use paramylon myristate as an all-natural pressure-sensitive adhesive (Shibakami and Sohma, 2018). Nickel accumulation by the green algae-like Euglena gracilis. Euglena gracilis growth and cell composition under different temperature, light and trophic conditions. . doi: 10.1016/j.biotechadv.2010.07.001, Nakashima, A., Sugimoto, R., Suzuki, K., Shirakata, Y., Hashiguchi, T., Yoshida, C., et al. (2009). 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). Crit. Rep. 28, 457466. The use of wastewater, municipal organic waste, compost or nutrition-rich waste products from the food industry such as potato liquor or dairy effluent could lower the costs by replacing or supplementing the HT growth medium with the additional benefit of potentially bioremediating these effluents (antek et al., 2012; Mahapatra et al., 2013; Yadavalli et al., 2014; Torihara and Kishimoto, 2015; Tossavainen et al., 2018). 97, 34943500. The alga Euglena gracilis (E. gracilis) has recently gained attention as a health food, but its effects on human gut microbiota remain unknown. The typical ascorbate titre of a PT-cultivated E. gracilis is around 4 mg/g DW or 8 mg/L culture, whereas it is negligible for E. gracilis cultivated under HT conditions (Shigeoka et al., 1980; Hasan et al., 2017). Large . 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). 84, 609612. J. Gene knockdown via RNA interference (RNAi) has led to the identification of the role of photoactivated adenylyl cyclase in phototaxis and the finding that glucan synthase-like 2 is essential for paramylon synthesis (Ntefidou et al., 2003; Tanaka et al., 2017). 7, 139147. 293, 28652876. Euglena gracilis is a freshwater species of single-celled alga in the genus Euglena. Euglena sp. doi: 10.1371/journal.pone.0191462, Takeda, T., Nakano, Y., Takahashi, M., Konno, N., Sakamoto, Y., Arashida, R., et al. Front. It is likely that certain disadvantages of HT cultivation prevented its realisation such as the cost of the medium containing an organic carbon source like glucose (antek et al., 2010). Advanced aviation fuels: a look ahead via a historical perspective. 58, 532538. Biomass Bioenergy 112, 138143. Prod. Prod. 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 live in fresh and brackish water habitats such as ponds rich in organic matter. At this time, microalgae-derived biofuels are not economically feasible because they are not competitive with fossil fuels due to their higher production costs. 16, 112. Phycol. of P. gracilis that may compromise the survival of this species but at higher concentrations than recorded in the environment, so P. gracilis can be considered tolerant to this herbicide at environmentally relevant concentrations. Biotechnol. ATCC 31749 by addition of low-polyphosphates. Food Sci. 12, 515520. Reported EPA and DHA titres in E. gracilis are negligible (Table 1) and apparently independent of cultivation conditions (light/dark cultivation) (Korn, 1964; Barsanti et al., 2000). doi: 10.1002/fsn3.383. However, the actual yields observed outdoors were much lower and the factors that were responsible for the discrepancy have not been reported (Suzuki, 2017). Eye Res. (1999). Functional characterization of D-galacturonic acid reductase, a key enzyme of the ascorbate biosynthesis pathway, from Euglena gracilis. Curr. Requirement for vitamin B1 for growth of Euglena gracilis. doi: 10.1016/0005-2744(67)90227-6, Matos, .P. 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 Biochemistry 42, 97799788. Vitaminol. Sci. (2018). Outdoor PT cultivation is considered the most economical option for the bulk production of microalgal biomass (Apel and Weuster-Botz, 2015). 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). 30, 19451955. Biochem. J. Biol. saccharophila. A promising approach to enhance microalgae productivity by exogenous supply of vitamins. This study aimed to determine the effect of E . 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). Nutraceuticals: opening the debate for a regulatory framework. doi: 10.1046/j.1529-8817.2001.037001038.x, Beacham, T.A., Sweet, J.B., and Allen, M.J. (2017). Isolation and characterization of paramylon synthase from Euglena gracilis (Euglenophyceae). There is an emerging market for E. gracilis-derived products, which is reflected in the recent founding of new companies specialised in the cultivation and commercialisation of E. gracilis. doi: 10.1023/a:1008022305865, Kusmic, C., Barsanti, L., Di Lascio, N., Faita, F., Evangelista, V., and Gualtieri, P. (2018).