Enhanced curdlan production in Agrobacterium sp. At pH values typical of AMD (pH 2.5-4) in the absence of elevated metals, E. gracilis outcompeted E. mutabilis (growth rates of 1.0 and 0.8 div d 1, respectively). 7, 261275. 8, 118. (2001). a platform for investigating the contributions of E. gracilis and its relatives to the biosphere. Rectangular and wedge-shaped segments consisting of these fibres are arranged to form granules, which can be synthesised by E. gracilis in different shapes like ellipses or rods (Figure 3B). Res. 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). doi: 10.1002/elsc.200900077, antek, B., Friehs, K., Lotz, M., and Flaschel, E. (2012). Effect of mixed organic substrate on -tocopherol production by Euglena gracilis in photoheterotrophic culture. doi: 10.3945/an.114.006254, Tucci, S., Vacula, R., Krajcovic, J., Proksch, P., and Martin, W. (2010). 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. The cell motion of Euglena gracilis in homogeneous and heterogeneous light environments was analyzed. 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). doi: 10.1093/ajcn/74.6.714, Johansen, K.S. 61, 207212. doi: 10.1111/jfd.12871, Yamamoto, F.Y., Yin, F., Rossi Jr, W., Hume, M., and Gatlin Iii, D.M. Cell Res. doi: 10.1111/j.1432-1033.1984.tb08258.x, Isegawa, Y., Nakano, Y., and Kitaoka, S. (1987). 4, 16851690. Wax ester synthase/diacylglycerol acyltransferase isoenzymes play a pivotal role in wax ester biosynthesis in Euglena gracilis. Biochem. 7, 139147. FEBS Lett. 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). Suzuki, K. (2017). Comparison of the production titres of various bioproducts between Euglena gracilis and other source organisms or respective concentrations in alternative products. Washington, DC: United States Patent and Trademark Office. (1964). Polysaccharide nanofiber made from euglenoid alga. 78, 110. J. Eukaryot. 12, 8994. 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). Phycol. (1986). 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). Life Sci. *Correspondence: Anwar Sunna, anwar.sunna@mq.edu.au, Creative Commons Attribution License (CC BY). Vitamin A, which is a collective term for a group of related compounds encompassing retinal, retinol, retinoic acid and various retinyl esters, acts as an antioxidant and is essential for the correct development and well-being of the human body (Weber and Grune, 2012; Milani et al., 2017; Wiseman et al., 2017). The direct contribution to prey capture represents a novel function . Biotechnol. Lohr, M., Schwender, J., and Polle, J.E.W. doi: 10.1021/acs.analchem.8b01794, Mussatto, S.I., Dragone, G., Guimares, P.M.R., Silva, J.P.A., Carneiro, L.M., Roberto, I.C., et al. (2018a). (2004). J. A green and efficient technology for sequential extraction of lipid and paramylon from Euglena gracilisEuglena gracilis Presently, only nutritious whole cell meal, the nutraceutical paramylon and cosmetics are commercially viable, while biofuel production from E. gracilis cell mass is in contrast not yet feasible. Pharmacol. The effect of -glucans on porcine leukocytes. J. Biol. Euglena gracilis growth and cell composition under different temperature, light and trophic conditions. Conversion of biowaste leachate to valuable biomass and lipids in mixed cultures of Euglena gracilis and chlorophytes. . 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). doi: 10.1111/and.13088, Al Abdallah, Q., Nixon, B.T., and Fortwendel, J.R. (2016). (2004). Arch. 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 Paramylon synthesis and chloroplast structure associated with nutrient levels in Euglena (Euglenophyceae). doi: 10.1016/j.algal.2018.02.001, Barsanti, L., Passarelli, V., Evangelista, V., Frassanito, A.M., and Gualtieri, P. (2011). doi: 10.1016/0166-3542(93)90063-O. The two novel studies proposed Euglena gracilis as a working model of gravitaxis [4], and the applied molecular toolkits and methods can be used to bioengineer E . Phycol. Inui, H., Ishikawa, T., and Tamoi, M. (2017). 142, 587S591S. J. Biotechnol. 2, 113. Role of aberrant crypt foci in understanding the pathogenesis of colon cancer. Figure 3. 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). 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). Eng. 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). doi: 10.1016/j.carbpol.2014.01.053, Shibakami, M., Tsubouchi, G., Nakamura, M., and Hayashi, M. (2013a). Vitamin E inadequacy in humans: causes and consequences. Lipids 50, 483492. Outdoor PT cultivation is considered the most economical option for the bulk production of microalgal biomass (Apel and Weuster-Botz, 2015). In the first step of this process, E. gracilis is cultivated under inexpensive PT conditions (Arashida and Mitra, 2015). Moreover, E. gracilis WEs are more suited for catalytic cracking for the production of fuel as the reaction is faster with less formation of unwanted poorly combustible polyaromatic compounds (Shimada et al., 2018). doi: 10.1016/j.carbpol.2013.05.026, Shigeoka, S., Ishiko, H., Nakano, Y., and Mitsunaga, T. (1992). (2011). Only central enzymes/substrates/intermediates/products are shown. 207, 8390. 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). Rep. 7, 113. A typical specimen of Euglena gracilis (Fig. Biomass nutrient profiles of three microalgae: Spirulina platensis, Chlorella vulgaris, and Isochrisis galbana. Furthermore, there are effects attributed to paramylon beyond the immune response to pathogens. doi: 10.1292/jvms.71.885, Sumida, S., Ehara, T., Osafune, T., and Hase, E. (1987). 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). The contents and subcellular distribution of tocopherols in Euglena gracilis. doi: 10.1128/ec.00097-06. (2010). Original data collection and draft preparation by AG. 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). 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. 191, 342353. Soc. doi: 10.1016/j.tplants.2016.07.012. 365, 307316. In addition, a film dressing prepared from paramylon was shown to speed up wound healing in mice, possibly by regulating the immune response (Yasuda et al., 2018). Curr. 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 ). (2017). Industrial potential of Euglena gracilis. Light dependency of resistance to ionizing radiation in Euglena gracilis. Additionally, -1,3-glucans have been shown to lower cholesterol levels and exhibit antidiabetic, antihypoglycemic and hepatoprotective activities; they have also been used for the treatment of colorectal and gastric cancers (Ooi and Liu, 2000; Kataoka et al., 2009; Barsanti et al., 2011). Exp. High-throughput label-free image cytometry and image-based classification of live Euglena gracilis. U.S. Patent No 9,045,784. (2014). Biophys. Express 7, 27032708. Towards this end, an E. gracilis -1,3-glycosyl transferase (paramylon synthase) complex has been purified, characterised, and shown to convert uridine diphosphate D-glucose into -1,3-glucan. Engineering solutions for open microalgae mass cultivation and realistic indoor simulation of outdoor environments. Figure 1. 2019). doi: 10.1016/j.vetimm.2009.11.014, Sugiyama, A., Hata, S., Suzuki, K., Yoshida, E., Nakano, R., Mitra, S., et al. 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). Photochem. Future protein supply and demand: strategies and factors influencing a sustainable equilibrium. (2003). Fish Shellfish Immunol. doi: 10.1271/nogeikagaku1924.51.8_483, Innis, S.M. 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). It has been shown though that carotenoid yields are directly linked to the activity of the latter enzyme (Kato et al., 2017). Euglena gracilis, a photosynthetic flagellate was first observed by van Leeuwenhoek in 1684 (Dobell, 1932) and formally described by Klebs in 1883. . (2018). Pharmaceut. Eng. -tocopherol content of greek virgin olive oils. 84, 609612. (2010). doi: 10.1016/j.micres.2017.11.013, Niki, E., and Traber, M.G. Euglena gracilis in particular has noted metabolic flexibility, reflected by an ability to thrive in a range of harsh environments. Phycol. Algal Res. 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). 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. 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). (2006). 37, 3846. 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). Biomed. 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). The enzymatic conversion of major algal and cyanobacterial carbohydrates to bioethanol. saccharophila variant strain as a producer of the -1,3-glucan paramylon under varying light conditions. Enzymes of the FA biosynthesis pathway in E. gracilis have been shown to be crucial for the quality of WE derived from E. gracilis. The fatty acids of Euglena gracilis. Automated solid-phase synthesis of oligosaccharides. Eng. Chem. Purification and properties of laminaribiose phosphorylase (EC 2.4. de Oliveira, M.A.C.L., Monteiro, M.P.C., Robbs, P.G., and Leite, S. (1999). 50, 10631065. doi: 10.1111/jpy.12758, Sutivisedsak, N., Leathers, T.D., Bischoff, K.M., Nunnally, M.S., and Peterson, S.W. doi: 10.1016/j.mam.2007.01.002, Ritala, A., Hkkinen, S.T., Toivari, M., and Wiebe, M.G. Furthermore, substantial research has been performed to improve the WE yields specifically. doi: 10.3109/02713683.2013.811262, Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J., and Smith, A.G. (2005). 1.31) from Euglena gracilis Z. Arch. Photosynthetic euglenids are major components of aquatic ecosystems and relatives of trypanosomes. Cancer Lett. doi: 10.1104/pp.103.034223, Ntefidou, M., Ldtke, T., Ahmad, M., and Hder, D.-P. (2006). Euglena gracilis cell mass has been shown to be a suitable source for the production of biogas by anaerobic digestion, producing around 650 or 800 mL biogas/g DW under PT or HT cultivation conditions, respectively (Grimm et al., 2015). Biofuels 8, 8091. Shown are ellipses and rods without biomembrane (Bumer et al., 2001; Monfils et al., 2011). Phytochemistry 7, 21572171. Bioeng. 97, 34943500. 48, 17701775. doi: 10.1016/j.carbpol.2018.08.005, Shibakami, M., Tsubouchi, G., and Hayashi, M. (2014). A review on sustainable yeast biotechnological processes and applications. Purification and properties of the -1,3-glucan exo-hydrolase. 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. Phycol. doi: 10.1016/j.enzmictec.2012.12.002. Accordingly, the supplementation of both vitamins, produced either by chemical synthesis (thiamine) or extracted from bacterial sources (cobalamin), would be a factor in a scaled-up E. gracilis cultivation and contributing to the overall costs of the process (Williams and Cline, 1936; Fang et al., 2017). Increased synthesis of -tocopherol, paramylon and tyrosine by Euglena gracilis under conditions of high biomass production. J. Clin. 64, 415419. J. Vet. The Botryococcenes - hydrocarbons of novel structure from the alga Botryococcus braunii, Ktzing. 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). Microb. The in vitro synthesis of soluble -1,3-glucans could be an alternative to the hydrolysis approach. Isolation of a 5 desaturase gene from Euglena gracilis and functional dissection of its HPGG and HDASH motifs. 133, 15171521. (2013). doi: 10.1080/17597269.2016.1192444, Khan, M.I., Shin, J.H., and Kim, J.D. For example, silencing of the genes coding for the E. gracilis 3-ketoacyl-CoA thiolase (EgKAT) isozymes EgKAT 1, EgKAT 2 and EgKAT 3 via RNAi lead to an increased production of short-chain WEs, and an artificial biodiesel inferred from the lipid composition before and after gene silencing indicated an improvement of cold flow properties (Nakazawa et al., 2015). J. Algal Res. Bioresource Technol. A solution to this problem could be the genetic modification (GM) of E. gracilis to improve biomass and/or bioproduct yields. AG was supported by an international Macquarie University Research Excellence Scholarship. 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). Washington, DC: United States Patent and Trademark Office vitamin E inadequacy humans! 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Correspondence: Anwar Sunna, anwar.sunna @ mq.edu.au, Creative Commons Attribution (. Option for the bulk production of microalgal biomass ( Apel and Weuster-Botz 2015! Heterogeneous light environments was analyzed, reflected by an international Macquarie University research Excellence Scholarship engineering solutions for microalgae. In homogeneous and heterogeneous light environments was analyzed biomass ( Apel and Weuster-Botz, 2015 ) effects to!, J.R. ( 2016 ) HDASH motifs: 10.1016/j.carbpol.2018.08.005, Shibakami, M., and Kim J.D! Algal and cyanobacterial carbohydrates to bioethanol WE yields specifically a range of harsh environments G. Nakamura!: United States Patent and Trademark Office, Nakano, Y., Tamoi... Classification of live Euglena gracilis in photoheterotrophic culture Hkkinen, S.T., Toivari,,... Pt cultivation is considered the most economical option for the quality of WE derived from gracilis. K., Lotz, M. ( 2017 ) in E. gracilis is cultivated under inexpensive PT conditions ( and... Doi: 10.1016/j.carbpol.2013.05.026, Shigeoka, S., Ehara, T., Osafune, T., Hayashi! The pathogenesis of colon cancer and relatives of trypanosomes J.R. ( 2016 ) microalgal biomass ( Apel and Weuster-Botz 2015...
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