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Suppression of DYRK ortholog expression affects wax ester fermentation in Euglena gracilis

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Abstract

In the microalga Euglena gracilis, the storage polysaccharide paramylon (β-1,3-D-glucan) is degraded to glucose, and finally converted to wax esters under anaerobic conditions. The wax esters and paramylon are now considered to be valuable materials for applications in biofuel production and in medicine. Genetic improvements of wax esters and paramylon accumulation in Euglena would facilitate their large-scale industrial applications; however, such improvements have thus far been difficult to realize because the regulatory factors involved in the wax ester fermentation pathway remain mostly unknown. Recently, two of dual-specificity Tyr phosphorylation-regulated kinases, starch degradation 1 (STD1) and triacylglycerol accumulation regulator 1 (TAR1), have been reported to regulate triacylglycerol metabolism in Chlamydomonas reinhardtii. In this study, we identified the Euglena DYRK orthologous sequences, and gene-silencing of EgSTD1 and EgSTD2 showed an increase in accumulation of paramylon and the following anaerobic wax ester production. This result indicated that EgSTD1 and EgSTD2 play a significant role in regulation of the wax ester fermentation pathway.

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References

  • Abbassi R, Johns TG, Kassiou M, Munoz L (2015) DYRK1A in neurodegeneration and cancer: molecular basis and clinical implications. Pharmacol Ther 151:87–98

    Article  CAS  PubMed  Google Scholar 

  • Aranda S, Laguna A, de la Luna S (2011) DYRK family of protein kinases: evolutionary relationships, biochemical properties, and functional roles. FASEB J 25:449–462

    Article  CAS  PubMed  Google Scholar 

  • Barallobre MJ, Perier C, Bové J et al (2014) DYRK1A promotes dopaminergic neuron survival in the developing brain and in a mouse model of Parkinson’s disease. Cell Death Dis 5:e1289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clarke AE, Stone BA (1960) Structure of the paramylon from Euglena gracilis. Biochim Biophys Acta 44:161–163

    Article  CAS  PubMed  Google Scholar 

  • Cranwell PA, Volkman JK (1981) Alkyl and steryl esters in a recent lacustrine sediment. Chem Geol 32:29–43

    Article  CAS  Google Scholar 

  • Grimme LH, Boardman NK (1972) Photochemical activities of a particle fraction P 1 obtained rom the green alga Chlorella fusca. Biochem Biophys Res Commun 49:1617–1623

    Article  CAS  PubMed  Google Scholar 

  • Hill HZ, Schiff JA, Epstein HT (1966) Studies of chloroplast development in Euglena: XIII. Variation of ultraviolet sensitivity with extent of chloroplast development. Biophys J 6:125–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inui H, Miyatake K, Nakano Y, Kitaoka S (1982) Wax ester fermentation in Euglena gracilis. FEBS Lett 150:89–93

    Article  CAS  Google Scholar 

  • Inui H, Miyatake K, Nakano Y, Kitaoka S (1983) Production and composition of wax esters by fermentation of Euglena gracilis. Agric Biol Chem 47:2669–2671

    CAS  Google Scholar 

  • Iseki M, Matsunaga S, Murakami A, Ohno K, Shiga K, Yoshida K, Sugai M, Takahashi T, Hori T, Watanabe M (2002) A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis. Nature 415:1047–1051

    Article  CAS  PubMed  Google Scholar 

  • Kajikawa M, Sawaragi Y, Shinkawa H, Yamano T, Ando A, Kato M, Hirono M, Sato N, Fukuzawa H (2015) Algal dual-specificity tyrosine phosphorylation-regulated kinase, triacylglycerol accumulation regulator1, regulates accumulation of triacylglycerol in nitrogen or sulfur deficiency. Plant Physiol 168:752–764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiss JZ, Roberts EM, Brown RM, Triemer RE (1988) X-ray and dissolution studies of paramylon storage granules from Euglena. Protoplasma 146:150–156

    Article  Google Scholar 

  • Knothe G (2008) “Designer” biodiesel: Optimizing fatty ester composition to improve fuel properties. Energy Fuel 22:1358–1364

    Article  CAS  Google Scholar 

  • Kondo Y, Kato A, Hojo H, Nozoe S, Takeuchi M, Ochi K (1992) Cytokine-related immunopotentiating activities of paramylon, a β-(1→3)-D-glucan from Euglena gracilis. Aust J Pharm 15:617–621

    CAS  Google Scholar 

  • Koren LE, Hutner SH (1967) High-yield media for photosynthesizing Euglena gracilis Z. J Protozool 14(Suppl):17

    Google Scholar 

  • Koritala S (1989) Microbiological synthesis of wax esters by Euglena gracilis. J Am Oil Chem Soc 66:133–134

    Article  CAS  Google Scholar 

  • Kuda T, Enomoto T, Yano T (2009) Effects of two storage β-1,3-glucans, laminaran from Eisenia bicyclis and paramylon from Euglena gracilis, on cecal environment and plasma lipid levels in rats. J Funct Foods 1:399–404

    Article  CAS  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Pohnert G, Wei D (2016) Extracellular metabolites from industrial microalgae and their biotechnological potential. Mar Drugs 14:191. doi:10.3390/md14100191

    Article  PubMed Central  Google Scholar 

  • Moriya H, Shimizu-Yoshida Y, Omori A, Iwashita S, Katoh M, Sakai A (2001) Yak1p, a DYRK family kinase, translocates to the nucleus and phosphorylates yeast Pop2p in response to a glucose signal. Genes Dev 15:1217–1228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy ASN, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25:3657–3683

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rosenberg A (1963) A comparison of lipid patterns in photosynthesizing and nonphotosynthesizing cells of Euglena gracilis. Biochemistry 2:1148–1154

    Article  CAS  PubMed  Google Scholar 

  • Russo R, Barsanti L, Evangelista V, Frassanito AM, Longo V, Pucci L, Penno G, Gualtieri P (2017) Euglena gracilis paramylon activates human lymphocytes by upregulating pro-inflammatory factors. Food Sci Nutr 5:205–214

    Article  CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schulz-Raffelt M, Chochois V, Auroy P, Cuiné S, Billon E, Dauvillée D, Li-Beisson Y, Peltier G (2016) Hyper-accumulation of starch and oil in a Chlamydomonas mutant affected in a plant-specific DYRK kinase. Biotechnol Biofuels 9:55. doi:10.1186/s13068-016-0469-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Shibakami M, Tsubouchi G, Sohma M, Hayashi M (2015) Preparation of transparent self-standing thin films made from acetylated euglenoid β-1,3-glucans. Carbohydr Polym 133:421–428

    Article  CAS  PubMed  Google Scholar 

  • Skurat AV, Dietrich AD (2004) Phosphorylation of Ser640 in muscle glycogen synthase by DYRK family protein kinases. J Biol Chem 279:2490–2498

    Article  CAS  PubMed  Google Scholar 

  • Tamaki S, Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2015) Biochemical and physiological analyses of NADPH-dependent thioredoxin reductase isozymes in Euglena gracilis. Plant Sci 236:29–36

    Article  CAS  PubMed  Google Scholar 

  • Tanaka Y, Ogawa T, Maruta T, Yoshida Y, Arakawa K, Ishikawa T (2017) Glucan synthase-like 2 is indispensable for paramylon synthesis in Euglena gracilis. FEBS Lett 591:1360–1370

    Article  CAS  PubMed  Google Scholar 

  • Teerawanichpan P, Qiu X (2010) Fatty acyl-CoA reductase and wax synthase from Euglena gracilis in the biosynthesis of medium-chain wax esters. Lipids 45:263–273

    Article  CAS  PubMed  Google Scholar 

  • Yoshida Y, Tomiyama T, Maruta T, Tomita M, Ishikawa T, Arakawa K (2016) De novo assembly and comparative transcriptome analysis of Euglena gracilis in response to anaerobic conditions. BMC Genomics 17:182. doi:10.1186/s12864-016-2540-6

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Yuji Tanaka, Ms. Kaeko Kurihara, Ms. Jun Luo, Dr. Takanori Maruta, and Dr. Takahisa Ogawa (Shimane University) for technical assistance and helpful discussions. This work was supported by CREST program from the JST.

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  1. Mitsuhiro Kimura

    Present address: Enzyme Research Team, Biomass Engineering Research Division, RIKEN Center for Sustainable Resource Science, 2-1 Hirosawa, Wako, Saitama, 351-0198, Japan

Authors and Affiliations

  1. Department of Life Science and Biotechnology, Faculty of Life and Environmental Science, Shimane University, 1060 Nishikawatsu, Matsue, Shimane, 690-8504, Japan

    Mitsuhiro Kimura & Takahiro Ishikawa

  2. Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency (JST), Saitama, Japan

    Mitsuhiro Kimura & Takahiro Ishikawa

Authors
  1. Mitsuhiro Kimura
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  2. Takahiro Ishikawa
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Correspondence to Takahiro Ishikawa.

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Kimura, M., Ishikawa, T. Suppression of DYRK ortholog expression affects wax ester fermentation in Euglena gracilis . J Appl Phycol 30, 367–373 (2018). https://doi.org/10.1007/s10811-017-1235-y

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  • DOI: https://doi.org/10.1007/s10811-017-1235-y

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