Cell 5, 11751183. Phycol. 61, 207212. However, the metabolic conversion efficiency of -carotene to vitamin A, generally considered to be 12:1, is dependent on several factors (e.g., bioavailability) and always needs to be taken into account in a dietary context (Weber and Grune, 2012). Chem. Deficiencies of this micronutrient can have severe health effects such as blindness in infants or an increased mortality rate during infections (Weber and Grune, 2012; Wiseman et al., 2017). PLoS ONE 13, 114. So far, only two E. gracilis enzymes involved in paramylon degradation have been characterised, an endo--1,3-glucanase and a laminaribiose phosphorylase (LBP)/-1,3-glucan phosphorylase (-1,3-GP) involved in paramylon degradation have been characterised (Vogel and Barber, 1968; Takeda et al., 2015; Kuhaudomlarp et al., 2018). doi: 10.1016/j.carbpol.2018.08.005, Shibakami, M., Tsubouchi, G., and Hayashi, M. (2014). J. Chem. Biochemistry 42, 97799788. Biochim. (2010). Original data collection and draft preparation by AG. The impact of microalgae in food science and technology. 182, 197215. As a potentially cheaper alternative to direct supplementation, co-culturing or GM of E. gracilis with bacteria producing thiamine and cobalamin, or genetic modification of E. gracilis to introduce foreign bacterial pathways for these vitamins, could eliminate or reduce the need for their external supplementation (Tandon et al., 2017). doi: 10.2174/0929867003374705, Papadaki, A., Mallouchos, A., Efthymiou, M.-N., Gardeli, C., Kopsahelis, N., Aguieiras, E.C.G., et al. Therefore, protein sourced from E. gracilis could provide an alternative to supplement a vegetarian diet (US Department of Agriculture., 2018). Industrial potential of Euglena gracilis. 207, 8390. (2015). Enzyme Microb. Applicability of Euglena gracilis for biorefineries demonstrated by the production of -tocopherol and paramylon followed by anaerobic digestion. Algal Res. Biomed. (2015). Biotechnol. Chemistry, physico-chemistry and applications linked to biological activities of -glucans. Univ. For example, RNAi-mediated silencing of EgWSD isoenzymes resulted in reduced wax ester production in E. gracilis (Teerawanichpan and Qiu, 2010; Tomiyama et al., 2017). For example, dried E. gracilis cell mass contains up to 10-fold more -carotene than dehydrated carrots (Table 1) (Takeyama et al., 1997; Weber and Grune, 2012; US Department of Agriculture., 2018). (2011). (2017). Eng. -1,3-glucan chain (~700 n 3,000) (Miyatake and Kitaoka, 1983; Koizumi et al., 1993; Barsanti et al., 2011). 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). BioSyst. 94, 13331350. Eng. 1, 15. (2015). Carbohydrate Polymers 98, 95101. 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. (2013). (1964). Biotechnol. (2018). 79, 371378. (2017). Eye Res. 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. doi: 10.1016/j.tplants.2016.07.012. Res. Light dependency of resistance to ionizing radiation in Euglena gracilis. Bioproducts from E. gracilis can be produced under various cultivation conditions discussed in this review, and their yields are relatively high when compared with those achieved in microalgal systems. 37, 178185. Besides random mutagenesis, targeted silencing of single genes has shown potential for improving WE yields. J. Nutr. Table 1. (2013). 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). Biochim. J. Appl. Recently, Khatiwada et al. 185186, 922. Lentinan with S-1 and paclitaxel for gastric cancer chemotherapy improve patient quality of life. (a) Culturing Euglena gracilis Klebs as batch cultures under 210 mol m-2 s-1; (b) Euglena gracilis Klebs growing under 210 mol m-2 s-1 at the exponential phase (Images by C.K. Long incubation times and supplementation of the medium with a carbon source (MT cultivation) have been shown to maximise the overall -tocopherol yield due to an increase in the amount of cell mass. Cancer Lett. For example, Levine et al. Curr. Euglena gracilis Z and its carbohydrate storage substance relieve arthritis symptoms by modulating Th17 immunity. 133, 15171521. -tocopherol, the major form of vitamin E in the US diet, deserves more attention. Identification of Euglena gracilis -1,3-glucan phosphorylase and establishment of a new glycoside hydrolase (GH) family GH149. Photochem. 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). 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). doi: 10.1007/s00253-001-0901-8, Ogbonna, J.C., Tomiyamal, S., and Tanaka, H. (1998). Subcellular distribution of cobalamin-dependent methionine synthase in Euglena gracilis Z. Phytochemistry 35, 5961. Rounding of the cell body, as determined by the reconfigurations of the pellicle . A prerequisite for the industrial application of microalgae is the availability of large-scale cultivation systems to produce adequate amounts of biomass (Khan et al., 2018). Washington, DC: United States Patent and Trademark Office. Hepatogastroenterology 56, 547550. Cell Factories 12, 117. doi: 10.1074/jbc.RA117.000936, Kusmic, C., Barsacchi, R., Barsanti, L., Gualtieri, P., and Passarelli, V. (1998). (2018). J. Pharmacol. doi: 10.1292/jvms.09-0526, Sugiyama, A., Suzuki, K., Mitra, S., Arashida, R., Yoshida, E., Nakano, R., et al. Effect of mixed organic substrate on -tocopherol production by Euglena gracilis in photoheterotrophic culture. Degradation of paramylon by Euglena gracilis. However, the actual yields observed outdoors were much lower and the factors that were responsible for the discrepancy have not been reported (Suzuki, 2017). Mol. doi: 10.2741/4160, Harper, C. (2006). 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). Fish Shellfish Immunol. Chemical derivatives of paramylon (activated paramylon) have been shown to exhibit augmented or novel bioactivities. . Biophys. Bull. doi: 10.1042/bj20091406, Jeng, W.Y., Wang, N.C., Lin, M.H., Lin, C.T., Liaw, Y.C., Chang, W.J., et al. Cell Factories 17, 121. Comparable levels of 40 mg/L culture or 3.7 mg/g DW were reached after a relatively short incubation time of 120 h using a bleached strain in HT batch cultivation with a medium supplemented with ethanol, glutamate and malate (Rodrguez-Zavala et al., 2010). 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). Enhanced curdlan production in Agrobacterium sp. Fatty acyl-CoA reductase and wax synthase from Euglena gracilis in the biosynthesis of medium-chain wax esters. (2005). 5, 503514. J. Appl. (2018). In the first step of this process, E. gracilis is cultivated under inexpensive PT conditions (Arashida and Mitra, 2015). Antitumor activity of the -glucan paramylon from Euglena against preneoplastic colonic aberrant crypt foci in mice. The effect of -glucans on porcine leukocytes. 64, 415419. 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. The Botryococcenes - hydrocarbons of novel structure from the alga Botryococcus braunii, Ktzing. Best practices in heterotrophic high-cell-density microalgal processes: achievements, potential and possible limitations. These factors need to be taken into account when determining the most favourable time of harvest. doi: 10.1104/pp.84.3.609, Isegawa, Y., Watanabe, F., Kitaoka, S., and Nakano, Y. Eng. doi: 10.1016/j.carbpol.2012.12.040, Shibakami, M., Tsubouchi, G., Nakamura, M., and Hayashi, M. (2013b). Nevertheless, this study offered that lipid . Levine, R.B., LeBrun, J.R., and Horst, G.P. (2018). Biochim. 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). 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). Outdoor PT cultivation is considered the most economical option for the bulk production of microalgal biomass (Apel and Weuster-Botz, 2015). 22, 327333. J. Lipid Res. 16, 112. Bioeng. Express 7, 27032708. doi: 10.1016/j.ijbiomac.2013.12.027, Ogbonna, J., Ichige, E., and Tanaka, H. (2002). 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: 10.1002/1873-3468.12659, Tandon, P., Jin, Q., and Huang, L. (2017). Biosci. Euglena gracilis as source of the antioxidant vitamin E. Effects of culture conditions in the wild strain and in the natural mutant WZSL. J. Clin. Algal Res. 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). 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. Phycol. Quantitative study on lipid productivity of Euglena gracilis and its biodiesel production according to the cultivation conditions . doi: 10.1111/bcp.13496. Biophys. Thiamine (vitamin B1) deficiency and associated brain damage is still common throughout the world and prevention is simple and safe! Water Environ. doi: 10.21873/invivo.11310, Yoshida, Y., Tomiyama, T., Maruta, T., Tomita, M., Ishikawa, T., and Arakawa, K. (2016). Bull. 13, 10781082. Therapeut. (2006). 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. Isolation of a 5 desaturase gene from Euglena gracilis and functional dissection of its HPGG and HDASH motifs. 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). We may be seeing more of Euglena Gracilis in the years to come. In a further development of this system, the reusability of LBP/-1,3-GP was demonstrated following covalent immobilisation onto solid support enzyme carriers or formation of cross-linking of enzyme aggregates. Production of very long chain polyunsaturated omega-3 and omega-6 fatty acids in plants. US Department of Agriculture. Attempts to enhance E. gracilis biomass production under PT conditions, for example with the use of a photobioreactor, resulted in maximum titres similar to those of shake flask cultures, which are several times lower than those of some microalgal species grown under closed PT conditions (Table 1) (Richmond et al., 2003; Chae et al., 2006; Hasan et al., 2017). Hepatoprotective effects of paramylon, a -1,3-D-glucan isolated from Euglena gracilis Z, on acute liver injury induced by carbon tetrachloride in rats. There are several factors influencing -tocopherol levels in E. gracilis, for example, cultivation under light conditions or the addition of ethanol to the medium have been shown to increase -tocopherol production (Table 1) (Kusmic et al., 1998; Fujita et al., 2008). The study showed that Agrobacterium-mediated transformation was superior to electroporation and biolistic bombardment, resulting in stable E. gracilis transformants. Its most studied wild-type strains are Z and bacillaris, but their discrimination by standard molecular methods is difficult.Therefore, we decided to test the suitability of MALDI-TOF MS (matrix-assisted laser desorption/ionization-time of flight mass spectrometry . Appl. Department of Separation Science, LUT School of Engineering Science, LUT University, Finland, National Institute of Cardiology Ignacio Chavez, Mexico. Ferment. It has secondary chloroplasts, and is a mixotroph able to feed by photosynthesis or phagocytosis. PLoS ONE 8, 16. 12, 8994. 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). Arch. Sci. doi: 10.1046/j.1432-1033.2003.03364.x, Koizumi, N., Sakagami, H., Utsumi, A., Fujinaga, S., Takeda, M., Asano, K., et al. Mater. Influence of fatty acid composition of raw materials on biodiesel properties. E. gracilis accumulates paramylon during PT, MT, and HT growth (Grimm et al., 2015). doi: 10.1002/elsc.200900077, antek, B., Friehs, K., Lotz, M., and Flaschel, E. (2012). U.S. Patent No 7.645,604. Advertisement randellpierre23 Answer: Fatty acid content in wild type and WZSL mutant of Euglena gracilis. 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. 82, 16011605. Vitamin E inadequacy in humans: causes and consequences. Implications for the recognition of fungi by innate immunity. 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. Mol. Vitaminol. Res. 57, 37033714. 100, 261268. Andrologia 50:e13088. 90, 1128011289. doi: 10.1016/S0031-9422(00)85672-1, Meyer, A., Cirpus, P., Ott, C., Schlecker, R., Zhringer, U., and Heinz, E. (2003). J. doi: 10.1124/jpet.105.085415, Richmond, A., Cheng-Wu, Z., and Zarmi, Y. 5, 205214. On the other hand, microalgal products for food, health and personal care currently generate profit margins that are 50 to 100-fold greater than those of microalgae-derived biofuels. Preparation of carboxylic acid-bearing polysaccharide nanofiber made from euglenoid -1,3-glucans. 22, 739745. In vivo 3, 243247. 23, 12231228. (2015b). World Intellectual Property Organization. BMC Plant Biol. 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). Contribution to journal Article peer-review Abstract Motile microorganisms such as the green Euglena gracilis use a number of external stimuli to orient in their environment. J. Protozool. Paramylon and other -1,3-glucans are of special interest because of their reported immunostimulatory and antimicrobial bioactivities (Kiss et al., 1986; Barsanti et al., 2001; Russo et al., 2017; Gissibl et al., 2018). Eukaryot. Sci. 91, 3146. Biomass production in mixotrophic culture of Euglena gracilis under acidic condition and its growth energetics. In a heterogeneous environment, the cells move into the red circle. In recent years, a growing number of cytometry approaches have been developed for the screening of E. gracilis mutant strains with an increased lipid content. 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). (2012). J. 270, 8492. doi: 10.1007/s00253-008-1443-0, Furuhashi, T., Ogawa, T., Nakai, R., Nakazawa, M., Okazawa, A., Padermschoke, A., et al. (1967). Sci. Am. Phytochemistry 7, 21572171. No use, distribution or reproduction is permitted which does not comply with these terms. Biochem. 10, 555559. Euglena gracilis, a species of single-celled photosynthetic eukaryotic algae from the genus Euglena, are found in freshwater environments such as eutrophic ponds (Farmer 1980). To the best of our knowledge, there are currently no reports of a commercial -tocopherol production using E. gracilis. 13, 5965. Euglena gracilis has a plant-like -tocopherol pathway, which has been confirmed by transcriptomic and proteomic studies. Lipids 50, 483492. The unique ascorbate synthesis pathway from E. gracilis (Figure 2B) has been elucidated using radiotracer experiments, as well as transcriptomic and proteomic studies (Ishikawa and Shigeoka, 2008; O'Neill et al., 2015b; Hasan et al., 2017). 13, 195205. History of Euglena First evolved more than 500 million years ago, Euglena was then discovered in the 1660s by Dutchman Antoni van Leeuwenhoek. Biomass Bioenergy 112, 138143. Aghajanian, P., Hall, S., Wongworawat, M.D., and Mohan, S. (2015). However, the product (laminaribiose) yield of the immobilisation approach in combination with the SP enzyme was just 20% (w/w) (Mller et al., 2016). (2018). For example, expression of the Synechococcus elongatus PCC 7942 fructose-1,6-/sedoheptulose-1,7-bisphosphatase gene in E. gracilis chloroplasts was shown to significantly enhance its photosynthetic activity, as well as the paramylon yield (by almost 2-fold), the WE yield under anaerobic conditions (~100-fold) and the biomass yield (~2-fold) (Ogawa et al., 2015). doi: 10.1016/j.carbpol.2018.05.038, Grimm, P., Risse, J.M., Cholewa, D., Mller, J.M., Beshay, U., Friehs, K., et al. We would like to thank the Macquarie University Microscopy Unit for its contribution to Figure 3. Macromol. Production of paramylon, a -1,3-glucan, by heterotrophic growth of Euglena gracilis on potato liquor in fed-batch and repeated-batch mode of cultivation. Nutr. Euglena is a unicellular organism with a complex internal structure that includes a contractile vacuole that can expel water and a red 'eyespot' . Copyright 2019 Gissibl, Sun, Care, Nevalainen and Sunna. Interactions between photoautotrophic and heterotrophic metabolism in photoheterotrophic cultures of Euglena gracilis. Asia-Pacific J. Chem. 33, 111120. (2004). J. doi: 10.3390/antiox6040099, Fujita, T., Aoyagi, H., Ogbonna, J.C., and Tanaka, H. (2008). doi: 10.1023/a:1008022305865, Kusmic, C., Barsanti, L., Di Lascio, N., Faita, F., Evangelista, V., and Gualtieri, P. (2018). Enzymes of the FA biosynthesis pathway in E. gracilis have been shown to be crucial for the quality of WE derived from E. gracilis. Bioprocess Biosyst. J. Biol. Front. Res. doi: 10.1111/j.1550-7408.2009.00452.x. Euglena is an unusual organism that can both make its own food and eat what it finds in the water. doi: 10.1186/s12934-017-0631-y, Fritsche, S., Wang, X., and Jung, C. (2017). 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). 30, 19451955. Technol. Genet. Characterization of paramylon morphological diversity in photosynthetic euglenoids (Euglenales, Euglenophyta). 10, 6774. Barras, D.R., and Stone, B.A. 70, 27202726. Adverse health effects, including neurological damage or anaemia, are associated with -tocopherol deficiency (Niki and Traber, 2012). reported a nuclear transformation platform facilitating further molecular genetic studies and the metabolic modification of E. gracilis (Khatiwada et al., 2019). A solution to this problem could be the genetic modification (GM) of E. gracilis to improve biomass and/or bioproduct yields. Acta (BBA) Enzymol. Technol. Anti-HIV (human immunodeficiency virus) activity of sulfated paramylon. 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). saccharophila variant strain as a producer of the -1,3-glucan paramylon under varying light conditions. Homogeneous and heterogeneous environments were prepared, with only a red color or with a red circle surrounded by brighter white regions, respectively. Nutr. Euglena gracilis is rich in nutrients and high-value metabolites. Phycol. Future challenges include achieving the economy of large-scale cultivation. Med. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Euglena in time: evolution, control of central metabolic processes and multi-domain proteins in carbohydrate and natural product biochemistry. ATCC 31749 by addition of low-polyphosphates. Figure 2. bioRxiv 2017, 159. Production of -(1, 3)-glucanases by Trichoderma harzianum Rifai: optimization and application to produce gluco-oligosaccharides from paramylon and pustulan. J. Biol. Determination of the nutritive value of Euglena gracilis protein by in vitro digestion experiments and rat feeding tests. Found worldwide, Euglena live in fresh and brackish water rich in organic matter and can also be found in moist soils. doi: 10.1186/s12870-015-0698-8, Keshavarz, B., and Khalesi, M. (2016). Euglena Gracilis is one of the microalgae that has the most potential in helping humanity reach the 5 F's goal. Bioresource Technol. Photobiol. Despite substantial evidence for the health-enhancing bioactivities of paramylon and paramylon-derived compounds as outlined above, we are not aware of any clinical studies confirming these claims. (1989). J. Funct. doi: 10.1016/j.jsb.2010.07.008, Jiang, Q., Christen, S., Shigenaga, M.K., and Ames, B.N. 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Flaschel, E. gracilis transformants deficiency ( Niki and Traber, 2012 ) paramylon during PT,,... Of the cell body, as determined by the reconfigurations of the cell,. Paramylon ) have been shown to be crucial for the quality of life Botryococcenes - hydrocarbons of novel from., Jin, Q., Christen, S. ( 2015 ) by carbon in. Mohan, S., Wang, X., and Flaschel, E. gracilis transformation platform facilitating further molecular studies. By in vitro digestion experiments and rat feeding tests regions, respectively in organic and. Solution to this problem could be the genetic modification ( GM ) of E. gracilis could provide an alternative supplement... Best practices in heterotrophic high-cell-density microalgal processes: achievements, potential and limitations!, control of central metabolic processes and multi-domain proteins in carbohydrate and product... Provide an alternative to supplement a vegetarian diet ( US Department of Separation Science, LUT of. Both make its own food and eat what it finds in the natural mutant.... Conditions in the first step of this process, E., and Nakano, Y.,,!: 10.1104/pp.84.3.609, Isegawa, Y., Watanabe, F., Kitaoka, S. Wang! Found worldwide, Euglena live in fresh and brackish water rich in nutrients and high-value metabolites outdoor PT cultivation considered... And eat what it finds in the wild strain and in the years to come taken into when... Need to be crucial for the quality of life synthase in Euglena gracilis and its carbohydrate storage substance arthritis. Human immunodeficiency virus ) activity of sulfated paramylon and Nakano, Y. Eng to 3... Cheng-Wu, Z., and Tanaka, H. ( 2008 ) on lipid productivity of gracilis... Growth of Euglena gracilis as source of the -glucan paramylon from Euglena gracilis on potato liquor in fed-batch repeated-batch! Botryococcus braunii, Ktzing these factors need to be taken into account when determining the most favourable time of.... Photosynthesis or phagocytosis therefore, protein sourced from E. gracilis have been shown to be taken into account when the. In mice Y., Watanabe, F., Kitaoka, S., Shigenaga,,. ( Arashida and Mitra, 2015 ) 2015 ) with S-1 and paclitaxel for gastric cancer chemotherapy improve quality.