Skip to main content
SpringerLink
Log in

Biochemistry and Physiology of Reactive Oxygen Species in Euglena

  • Chapter
  • First Online:
Euglena: Biochemistry, Cell and Molecular Biology

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 979))

Abstract

Reactive oxygen species (ROS) such as superoxide and hydrogen peroxide are by-products of various metabolic processes in aerobic organisms including Euglena. Chloroplasts and mitochondria are the main sites of ROS generation by photosynthesis and respiration, respectively, through the active electron transport chain. An efficient antioxidant network is required to maintain intracellular ROS pools at optimal conditions for redox homeostasis. A comparison with the networks of plants and animals revealed that Euglena has acquired some aspects of ROS metabolic process. Euglena lacks catalase and a typical selenocysteine containing animal-type glutathione peroxidase for hydrogen peroxide scavenging, but contains enzymes involved in ascorbate-glutathione cycle solely in the cytosol. Ascorbate peroxidase in Euglena, which plays a central role in the ascorbate-glutathione cycle, forms a unique intra-molecular dimer structure that is related to the recognition of peroxides. We recently identified peroxiredoxin and NADPH-dependent thioredoxin reductase isoforms in cellular compartments including chloroplasts and mitochondria, indicating the physiological significance of the thioredoxin system in metabolism of ROS. Besides glutathione, Euglena contains the unusual thiol compound trypanothione, an unusual form of glutathione involving two molecules of glutathione joined by a spermidine linker, which has been identified in pathogenic protists such as Trypanosomatida and Schizopyrenida. Furthermore, in contrast to plants, photosynthesis by Euglena is not susceptible to hydrogen peroxide because of resistance of the Calvin cycle enzymes fructose-1,6-bisphosphatse, NADP+-glyceraldehyde-3-phosphatase, sedoheptulose-1,7-bisphosphatase, and phosphoribulokinase to hydrogen peroxide. Consequently, these characteristics of Euglena appear to exemplify a strategy for survival and adaptation to various environmental conditions during the evolutionary process of euglenoids.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

AOX:

Alternative oxidase

APX:

Ascorbate peroxidase

AsA:

L-ascorbic acid

DHA:

Dehydroascorbate

DHAR:

Dehydroascorbate reductase

FBPase:

Fructose-1,6-bisphosphatse

FTR:

Ferredoxin-dependent Trx reductase

GAPDH:

Glyceralgehyde-3-phosphate dehydrogenase

GPX:

Glutathione peroxidase

GR:

Glutathione reductase

GSH:

Reduced glutathione

GSH1:

γ-glutamylcysteine synthetase

GSH2:

Glutathione synthetase

GSP:

Glutathionylspermidine

GSPS:

Glutathionylspermidine synthetase

GSSG:

Oxidized glutathione

MDA:

Monodehydroascorbate

MDAR:

Monodehydroascorbate reductase

NTR:

NADPH-dependent Trx reductase

OvoA:

5-histidylcysteine sulfoxide synthase

Prx:

Peroxiredoxin

PSI:

Photosystem I

PSII:

Photosystem II

ROS:

Reactive oxygen species

RuPK:

Ribulose-5-phosphate kinase

SBPase:

Sedoheptulose-1,7-bisphosphatase

SOD:

Super oxide dismutase

Srx:

Sulfiredoxin

T(SH)2 :

Trypanothione

Trx:

Thioredoxin

TRYR:

Trypanothione reductase

γ-EC:

γ-Glu-Cys

References

  • Arnér ES, Holmgren A (2000) Physiological functions of thioredoxin and thioredoxin reductase. Eur J Biochem 267:6102–6109

    Article  PubMed  Google Scholar 

  • Ariyanayagam MR, Fairlamb AH (2001) Ovothiol and trypanothione as antioxidants in trypanosomatids. Mol Biochem Parasitol 115:189–198

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Kanematsu S, Uchida K (1977) Superoxide dismutases in photosynthetic organisms: absence of the cuprozinc enzyme in eukaryotic algae. Arch Biochem Biophys 179:243–256

    Article  CAS  PubMed  Google Scholar 

  • Asada K, Badger MR (1984) Photoreduction of 18O2 and H2 18O2 with concomitant evolution of 16O2 in intact spinach chloroplasts: evidence for scavenging of hydrogen peroxide by peroxidase. Plant Cell Physiol 25:1169–1179

    CAS  Google Scholar 

  • Asada K (1992a) Production and scavenging of active oxygen species in chloroplasts. In: Scandalios JG (ed) Molecular Biology of Free Radical Scavenging Systems: Current Communications in Cell and Molecular Biology, vol 5. CSHL Press, New York, pp 173–192

    Google Scholar 

  • Asada K (1992b) Ascorbate peroxidase – a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

    Article  CAS  Google Scholar 

  • Bleier L, Dröse S (2013) Superoxide generation by complex III: From mechanistic rationales to functional consequences. Biochim Biophys Act 1827:1320–1331

    Article  CAS  Google Scholar 

  • Braunshausen A, Seebeck FP (2011) Identification and characterization of the first ovothiol biosynthetic enzyme. J Am Chem Soc 133:1757–1759

    Article  CAS  PubMed  Google Scholar 

  • Castro H, Sousa C, Novais M, Santos M, Budde H, Cordeiro-da-Silva A, Flohé L, Tomás AM (2004) Two linked genes of Leishmania infantum encode tryparedoxins localised to cytosol and mitochondrion. Mol Biochem Parasitol 136:137–147

    Article  CAS  PubMed  Google Scholar 

  • Cejudo FJ, Ferrández J, Cano B, Puerto-Galán L, Guinea M (2012) The function of the NADPH thioredoxin reductase C-2-Cys peroxiredoxin system in plastid redox regulation and signaling. FEBS Lett 586:2974–2980

    Article  CAS  PubMed  Google Scholar 

  • Cha JY, Kim JY, Jung IJ, Kim MR, Melencion A, Alam SS, Yun DJ, Lee SY, Kim MG, Kim WY (2014) NADPH-dependent thioredoxin reductase A (NTRA) confers elevated tolerance to oxidative stress and drought. Plant Physiol Biochem 80:184–191

    Article  CAS  PubMed  Google Scholar 

  • Chew O, Whelan J, Millar AH (2003) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869–46877

    Article  CAS  PubMed  Google Scholar 

  • Dietz KJ (2003) Plant peroxiredoxins. Annu Rev Plant Biol 54:93–107

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Liu Y, Jian JC, Wu ZH, Miao JL (2012) Molecular cloning and expression analysis of glutathione reductase gene in Chlamydomonas sp. ICE-L from Antarctica. Mar Genomics 5:59–64

    Article  PubMed  Google Scholar 

  • Durnford DG, Gray MW (2006) Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryot Cell 5:2079–2091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes AP, Holmgren A (2004) Glutaredoxins: glutathione-dependent redox enzymes with functions far beyond a simple thioredoxin backup system. Antioxid Redox Signal 6:63–74

    Article  CAS  PubMed  Google Scholar 

  • Fischer BB, Dayer R, Schwarzenbach Y, Lemaire SD, Behra R, Liedtke A, Eggen RI (2009) Function and regulation of the glutathione peroxidase homologous gene GPXH/GPX5 in Chlamydomonas reinhardtii. Plant Mol Biol 71:569–583

    Article  CAS  PubMed  Google Scholar 

  • Fischer BB, Ledford HK, Wakao S, Huang SG, Casero D, Pellegrini M, Merchant SS, Koller A, Eggen RI, Niyogi KK (2012) SINGLET OXYGEN RESISTANT 1 links reactive electrophile signaling to singlet oxygen acclimation in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 109:E1302–E1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Flohé L (2012) The trypanothione system and the opportunities it offers to create drugs for the neglected kinetoplast diseases. Biotechnol Adv 30:294–301

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Funato Y, Miki H (2010) Redox regulation of Wnt signalling via nucleoredoxin. Free Radic Res 44:379–388

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Anjum NA, Hasanuzzaman M, Gill R, Trivedi DK, Ahmad I, Pereira E, Tuteja N (2013) Glutathione and glutathione reductase: a boon in disguise for plant abiotic stress defense operations. Plant Physiol Biochem 70:204–212

    Article  CAS  PubMed  Google Scholar 

  • Grace SC (1990) Phylogenetic distribution of superoxide dismutase supports an endosymbiotic origin for chloroplasts and mitochondria. Life Sci 47:1875–1886

    Article  CAS  PubMed  Google Scholar 

  • Hofmann B, Budde H, Bruns K, Guerrero SA, Kalisz HM, Menge U, Montemartini M, Nogoceke E, Steinert P, Wissing JB, Flohé L, Hecht HJ (2001) Structures of tryparedoxins revealing interaction with trypanothione. Biol Chem 382:459–471

    Article  CAS  PubMed  Google Scholar 

  • Holmgren A, Sengupta R (2010) The use of thiols by ribonucleotide reductase. Free Radic Biol Med 49:1617–1628

    Article  CAS  PubMed  Google Scholar 

  • Iglesias-Baena I, Barranco-Medina S, Sevilla F, Lázaro JJ (2011) The dual-targeted plant sulfiredoxin retroreduces the sulfinic form of atypical mitochondrial peroxiredoxin. Plant Physiol 155:944–955

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa T, Takeda T, Shigeoka S, Hirayama O, Mitsunaga T (1993a) Hydrogen peroxide generation in organelles of Euglena gracilis. Phytochemistry 33:1297–1299

    Article  CAS  Google Scholar 

  • Ishikawa T, Takeda T, Shigeoka S, Hirayama O, Mitsunaga T (1993b) Requirement for iron and its effect on ascorbate peroxidase in Euglena gracilis. Plant Sci 93:25–29

    Article  CAS  Google Scholar 

  • Ishikawa T, Takeda T, Kohno H, Shigeoka S (1996) Molecular characterization of Euglena ascorbate peroxidase using monoclonal antibody. Biochim Biophys Acta 1290:69–75

    Article  PubMed  Google Scholar 

  • Ishikawa T, Madhusudhan R, Shigeoka S (2003) Effect of iron on the expression of ascorbate peroxidase in Euglena gracilis. Plant Sci 165:1363–1376

    Article  CAS  Google Scholar 

  • Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa T, Nishikawa H, Gao Y, Sawa Y, Shibata H, Yabuta Y, Maruta T, Shigeoka S (2008) The pathway via D-galacturonate/L-galactonate is significant for ascorbate biosynthesis in Euglena gracilis: identification and functional characterization of aldonolactonase. J Biol Chem 283:31133–31141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishikawa T, Tajima N, Nishikawa H, Gao Y, Rapolu M, Shibata H, Sawa Y, Shigeoka S (2010) Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: its unique molecular characterization. Biochem J 426:125–134

    Article  CAS  PubMed  Google Scholar 

  • Jacquot JP, Eklund H, Rouhier N, Schürmann P (2009) Structural and evolutionary aspects of thioredoxin reductases in photosynthetic organisms. Trends Plant Sci 14:336–343

    Article  CAS  PubMed  Google Scholar 

  • Jasso-Chávez R, Pacheco-Rosales A, Lira-Silva E, Gallardo-Pérez JC, García N, Moreno-Sánchez R (2010) Toxic effects of Cr(VI) and Cr(III) on energy metabolism of heterotrophic Euglena gracilis. Aquat Toxicol 100:329–338

    Article  PubMed  CAS  Google Scholar 

  • Jones DC, Ariza A, Chow WH, Oza SL, Fairlamb AH (2010) Comparative structural, kinetic and inhibitor studies of Trypanosoma brucei trypanothione reductase with T. cruzi. Mol Biochem Parasitol 169:12–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaiser WM (1979) Reversible inhibition of the Calvin cycle and activation of the oxidative pentose phosphate cycle in isolated intact chloroplasts by hydrogen peroxide. Planta 145:377–382

    Article  CAS  PubMed  Google Scholar 

  • Kanematsu S, Asada K (1979) Ferric and manganic superoxide dismutases in Euglena gracilis. Arch Biochem Biophys 195:535–545

    Article  CAS  PubMed  Google Scholar 

  • Kato S, Takaichi S, Ishikawa T, Asahina M, Takahashi S, Shinomura T (2016) Identification and functional analysis of the geranylgeranyl pyrophosphate synthase gene (crtE) and phytoene synthase gene (crtB) for carotenoid biosynthesis in Euglena gracilis. BMC Plant Biol 16:4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim C, Apel K (2013) Singlet oxygen-mediated signaling in plants: moving from flu to wild type reveals an increasing complexity. Photosynth Res 116:455–464

    Article  CAS  PubMed  Google Scholar 

  • Kottuparambil S, Shin W, Brown MT, Han T (2012) UV-B affects photosynthesis, ROS production and motility of the freshwater flagellate, Euglena agilis Carter. Aquat Toxicol 122-123:206–213

    Article  CAS  PubMed  Google Scholar 

  • Lord JM, Merrett MJ (1971) The intracellular localization of glycollate oxidoreductase in Euglena gracilis. Biochem J 124:275–281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Post-transcriptional regulation of ascorbate peroxidase during light adaptation of Euglena gracilis. Plant Sci 165:233–238

    Article  CAS  Google Scholar 

  • Manta B, Comini M, Medeiros A, Hugo M, Trujillo M, Radi R (2013) Trypanothione: a unique bis-glutathionyl derivative in trypanosomatids. Biochim Biophys Acta 1830:3199–3216

    Article  CAS  PubMed  Google Scholar 

  • Marchal C, Delorme-Hinoux V, Bariat L, Siala W, Belin C, Saez-Vasquez J, Riondet C, Reichheld JP (2014) NTR/NRX define a new thioredoxin system in the nucleus of Arabidopsis thaliana cells. Mol Plant 7:30–44

    Article  CAS  PubMed  Google Scholar 

  • Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2016) Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant Cell Physiol 57:1377–1386

    CAS  PubMed  Google Scholar 

  • Mendoza-Cozatl D, Devars S, Loza-Tavera H, Moreno-Sánchez R (2002) Cadmium accumulation in the chloroplast of Euglena gracilis. Physiol Plant 115:276–283

    Article  CAS  PubMed  Google Scholar 

  • Michelet L, Zaffagnini M, Morisse S, Sparla F, Pérez-Pérez ME, Francia F, Danon A, Marchand CH, Fermani S, Trost P, Lemaire SD (2013) Redox regulation of the Calvin-Benson cycle: something old, something new. Front Plant Sci 4:470

    Article  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Poulos TL (2005) Ascorbate peroxidase. In: Smirnoff N (ed) Antioxidants and Reactive Oxygen Species in Plants. Blackwell, Oxford, pp 87–100

    Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K et al (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Miyake C, Michihata F, Asada K (1991) Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: acquisition of ascorbate peroxidase during the evolution of Cyanobacteria. Plant Cell Physiol 32:33–43

    CAS  Google Scholar 

  • Montrichard F, Le Guen F, Laval-Martin DL, Davioud-Charvet E (1999) Evidence for the co-existence of glutathione reductase and trypanothione reductase in the non-trypanosomatid Euglenozoa: Euglena gracilis Z. FEBS Lett 442:29–33

    Article  CAS  PubMed  Google Scholar 

  • Mubarakshina MM, Ivanov BN, Naydov IA, Hillier W, Badger MR, Krieger-Liszkay A (2010) Production and diffusion of chloroplastic H2O2 and its implication to signalling. J Exp Bot 61:3577–3587

    Article  CAS  PubMed  Google Scholar 

  • Müller S, Liebau E, Walter RD, Krauth-Siegel RL (2003) Thiol-based redox metabolism of protozoan parasites. Trends Parasitol 19:320–328

    Article  PubMed  CAS  Google Scholar 

  • Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417:1–13

    Article  CAS  PubMed  Google Scholar 

  • Najami N, Janda T, Barriah W, Kayam G, Tal M, Guy M, Volokita M (2008) Ascorbate peroxidase gene family in tomato: its identification and characterization. Mol Gen Genomics 279:171–182

    Article  CAS  Google Scholar 

  • Navrot N, Collin V, Gualberto J, Gelhaye E, Hirasawa M, Rey P, Knaff DB, Issakidis E, Jacquot JP, Rouhier N (2006) Plant glutathione peroxidases are functional peroxiredoxins distributed in several subcellular compartments and regulated during biotic and abiotic stresses. Plant Physiol 142:1364–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa T, Kimura A, Sakuyama H, Tamoi M, Ishikawa T, Shigeoka S (2015) Characterization and physiological role of two types of chloroplastic fructose-1,6-bisphosphatases in Euglena gracilis. Arch Biochem Biophys 575:61–68

    Article  CAS  PubMed  Google Scholar 

  • Ogbonna JC (2009) Microbiological production of tocopherols: current state and prospects. Appl Microbiol Biotechnol 84:217–225

    Article  CAS  PubMed  Google Scholar 

  • O'Neill EC, Trick M, Hill L, Rejzek M, Dusi RG, Hamilton CJ, Zimba PV, Henrissat B, Field RA (2015) The transcriptome of Euglena gracilis reveals unexpected metabolic capabilities for carbohydrate and natural product biochemistry. Mol BioSyst 11:2808–2820

    Article  PubMed  CAS  Google Scholar 

  • Overbaugh JM, Fall R (1985) Characterization of a selenium-independent glutathione peroxidase from Euglena gracilis. Plant Physiol 77:437–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oza SL, Tetaud E, Ariyanayagam MR, Warnon SS, Fairlamb AH (2002) A single enzyme catalyses formation of Trypanothione from glutathione and spermidine in Trypanosoma cruzi. J Biol Chem 277:35853–35861

    Article  CAS  PubMed  Google Scholar 

  • Palmer H, Ohta M, Watanabe M, Suzuki T (2002) Oxidative stress-induced cellular damage caused by UV and methyl viologen in Euglena gracilis and its suppression with rutin. J Photochem Photobiol B 67:116–129

    Article  CAS  PubMed  Google Scholar 

  • Piñeyro MD, Parodi-Talice A, Portela M, Arias DG, Guerrero SA, Robello C (2011) Molecular characterization and interactome analysis of Trypanosoma cruzi tryparedoxin 1. J Proteome 74:1683–16892

    Article  CAS  Google Scholar 

  • Pujol-Carrion N, Belli G, Herrero E, Nogues A, de la Torre-Ruiz MA (2006) Glutaredoxins Grx3 and Grx4 regulate nuclear localisation of Aft1 and the oxidative stress response in Saccharomyces cerevisiae. J Cell Sci 119:4554–4564

    Article  CAS  PubMed  Google Scholar 

  • Purvis AC (1997) Role of the alternative oxidase in limiting superoxide production by plant mitochondria. Physiol Plant 100:165–170

    Article  CAS  Google Scholar 

  • Reichheld JP, Khafif M, Riondet C, Droux M, Bonnard G, Meyer Y (2007) Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development. Plant Cell 19:1851–1865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roach T, Miller R, Aigner S, Kranner I (2015) Diurnal changes in the xanthophyll cycle pigments of freshwater algae correlate with the environmental hydrogen peroxide concentration rather than non-photochemical quenching. Ann Bot 116:519–527

    Article  PubMed  PubMed Central  Google Scholar 

  • Rocchetta I, Küpper H (2009) Chromium- and copper-induced inhibition of photosynthesis in Euglena gracilis analysed on the single-cell level by fluorescence kinetic microscopy. New Phytol 182:405–420

    Article  CAS  PubMed  Google Scholar 

  • Rocchetta I, Mazzuca M, Conforti V, Balzaretti V, del Carmen Ríos de Molina M. (2012) Chromium induced stress conditions in heterotrophic and auxotrophic strains of Euglena gracilis. Ecotoxicol Environ Saf 84: 147–154

    Google Scholar 

  • Rodríguez-Zavala JS, García-García JD, Ortiz-Cruz MA, Moreno-Sánchez R (2007) Molecular mechanisms of resistance to heavy metals in the protist Euglena gracilis. J Environ Sci Health A Tox Hazard Subst Environ Eng 42:1365–1378

    Article  PubMed  CAS  Google Scholar 

  • Rouhier N, Jacquot JP (2005) The plant multigenic family of thiol peroxidases. Free Radic Biol Med 38:1413–1421

    Article  CAS  PubMed  Google Scholar 

  • Rouhier N, Couturier J, Johnson MK, Jacquot JP (2010) Glutaredoxins: roles in iron homeostasis. Trends Biochem Sci 35:43–52

    Article  CAS  PubMed  Google Scholar 

  • Ruggeri BA, Gray RJ, Watkins TR, Tomlins RI (1985) Effects of low-temperature acclimation and oxygen stress on tocopheron production in Euglena gracilis Z. Appl Environ Microbiol 50:1404–1408

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schürmann P, Jacquot JP (2000) Plant thioredoxin systems revisited. Annu Rev Plant Physiol Plant Mol Biol 51:371–400

    Article  PubMed  Google Scholar 

  • Schürmann P, Buchanan BB (2008) The ferredoxin/thioredoxin system of oxygenic photosynthesis. Antioxid Redox Signal 10:1235–1274

    Article  PubMed  Google Scholar 

  • Schmidtmann E, König AC, Orwat A, Leister D, Hartl M, Finkemeier I (2014) Redox regulation of Arabidopsis mitochondrial citrate synthase. Mol Plant 7:156–169

    Article  CAS  PubMed  Google Scholar 

  • Serrato AJ, Pérez-Ruiz JM, Spínola MC, Cejudo FJ (2004) A novel NADPH thioredoxin reductase, localized in the chloroplast, which deficiency causes hypersensitivity to abiotic stress in Arabidopsis thaliana. J Biol Chem 279:43821–43827

    Article  CAS  PubMed  Google Scholar 

  • Sevilla F, Camejo D, Ortiz-Espín A, Calderón A, Lázaro JJ, Jiménez A (2015) The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J Exp Bot 66:2945–2955

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Yokota A, Nakano Y, Kitaoka S (1979) The effect of illumination on the L-ascorbic acid content in Euglena gracilis Z. Agric Biol Chem 43:2053–2058

    CAS  Google Scholar 

  • Shigeoka S, Nakano Y, Kitaoka S (1980a) Purification and some properties of L-ascorbic-acid-specific peroxidase in Euglena gracilis Z. Arch Biochem Biophys 201:121–127

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Nakano Y, Kitaoka S (1980b) Metabolism of hydrogen peroxide in Euglena gracilis Z by L-ascorbic acid peroxidase. Biochem J 186:377–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeoka S, Onishi T, Nakano Y, Kitaoka S (1987a) Photoinduced biosynthesis of glutathione in Euglena gracilis. Agric Biol Chem 51:2257–2258

    CAS  Google Scholar 

  • Shigeoka S, Yasumoto R, Onishi T, Nakano Y, Kitaoka S (1987b) Properties of monodehydroascirbate reductase and dehydroascorbate reductase and their participation in the regeneration of ascorbate in Euglena gracilis. J Gen Microbiol 133:227–232

    CAS  Google Scholar 

  • Shigeoka S, Onishi T, Nakano Y, Kitaoka S (1987c) Characterization and physiological function of glutathione reductase in Euglena gracilis Z. Biochem J 242:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeoka S, Takeda T, Hanaoka T (1991) Characterization and immunological properties of selenium-containing glutathione peroxidase induced by selenite in Chlamydomonas reinhardtii. Biochem J 275:623–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shigeoka S, Ishiko H, Nakano Y, Mitsunaga T (1992) Isolation and properties of gamma-tocopherol methyltransferase in Euglena gracilis. Biochim Biophys Acta 1128:220–226

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Maruta T (2014) Cellular redox regulation, signaling, and stress response in plants. Biosci Biotechnol Biochem 78:1457–1470

    Article  CAS  PubMed  Google Scholar 

  • Sies H (2014) Role of metabolic H2O2 generation: redox signaling and oxidative stress. J Biol Chem 289:8735–8741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith K, Opperdoes FR, Fairlamb AH (1991) Subcellular distribution of trypanothione reductase in bloodstream and procyclic forms of Trypanosoma brucei. Mol Biochem Parasitol 48:109–112

    Article  CAS  PubMed  Google Scholar 

  • Takaichi S (2011) Carotenoids in algae: distributions, biosyntheses and functions. Mar Drugs 9:1101–1118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeda T, Yokota A, Shigeoka S (1995) Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol 36:1089–1095

    Article  CAS  Google Scholar 

  • Tamaki S, Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2014) Identification and functional analysis of peroxiredoxin isoforms in Euglena gracilis. Biosci Biotechnol Biochem 78:593–601

    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 

  • Teixeira FK, Menezes-Benavente L, Margis R, Margis-Pinheiro M (2004) Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: inferences from the rice genome. J Mol Evol 59:761–770

    Article  CAS  PubMed  Google Scholar 

  • Tetaud E, Manai F, Barrett MP, Nadeau K, Walsh CT, Fairlamb AH (1998) Cloning and characterization of the two enzymes responsible for trypanothione biosynthesis in Crithidia fasciculata. J Biol Chem 273:19383–19390

    Article  CAS  PubMed  Google Scholar 

  • Torrents E, Trevisiol C, Rotte C, Hellman U, Martin W, Reichard P (2006) Euglena gracilis ribonucleotide reductase: the eukaryote class II enzyme and the possible antiquity of eukaryote B12 dependence. J Biol Chem 281:5604–5611

    Article  CAS  PubMed  Google Scholar 

  • Vandenabeele S, Vanderauwera S, Vuylsteke M, Rombauts S, Langebartels C, Seidlitz HK, Zabeau M, Van Montagu M, Inzé D, Van Breusegem F (2004) Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana. Plant J 39:45–58

    Article  CAS  PubMed  Google Scholar 

  • Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wakabayashi K (2009) Analysis of redox-sensitive dynein components. Methods Cell Biol 92:153–161

    Article  CAS  PubMed  Google Scholar 

  • Wakabayashi K, Misawa Y, Mochiji S, Kamiya R (2011) Reduction-oxidation poise regulates the sign of phototaxis in Chlamydomonas reinhardtii. Proc Natl Acad Sci U S A 108:11280–11284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wakao S, Chin BL, Ledford HK, Dent RM, Casero D, Pellegrini M, Merchant SS, Niyogi KK (2014) Phosphoprotein SAK1 is a regulator of acclimation to singlet oxygen in Chlamydomonas reinhardtii. elife 3:e02286

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watanabe M, Suzuki T (2002) Involvement of reactive oxygen stress in cadmium-induced cellular damage in Euglena gracilis. Comp Biochem Physiol C Toxicol Pharmacol 131:491–500

    Article  PubMed  Google Scholar 

  • Wheeler G, Ishikawa T, Pornsaksit V, Smirnoff N (2015) Evolution of alternative biosynthetic pathways for vitamin C following plastid acquisition in photosynthetic eukaryotes. elife 4:e06369

    PubMed Central  Google Scholar 

  • Wood ZA, Schröder E, Robin Harris J, Poole LB (2003) Structure, mechanism and regulation of peroxiredoxins. Trends Biochem Sci 28:32–40

    Article  CAS  PubMed  Google Scholar 

  • Yokota Y, Nakano Y, Kitaoka S (1978) Metabolism of glycolate in mitochondria of Euglena gracilis. Agric Biol Chem 42:121–129

    CAS  Google Scholar 

  • Yokota A, Kawabata A, Kitaoka S (1983) Mechanism of glyoxylate decarboxylation in the glycolate pathway in Euglena gracilis Z: participation of Mn2+-dependent NADPH oxidase in chloroplasts. Plant Physiol 71:772–776

    Article  CAS  PubMed  PubMed Central  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zaffagnini M, Michelet L, Massot V, Trost P, Lemaire SD (2008) Biochemical characterization of glutaredoxins from Chlamydomonas reinhardtii reveals the unique properties of a chloroplastic CGFS-type glutaredoxin. J Biol Chem 283:8868–8876

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Bond CS, Bailey S, Cunningham ML, Fairlamb AH, Hunter WN (1996) The crystal structure of trypanothione reductase from the human pathogen Trypanosoma cruzi at 2.3 Ã… resolution. Protein Sci 5:52–61

    Article  PubMed  PubMed Central  Google Scholar 

  • Ziemann M, Bhave M, Zachgo S (2009) Origin and diversification of land plant CC-type glutaredoxins. Genome Biol Evol 1:265–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

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

    Takahiro Ishikawa, Shun Tamaki & Takanori Maruta

  2. Faculty of Agriculture, Kindai University, 3327-204 Nakamachi, Nara, 631-8505, Japan

    Shigeru Shigeoka

Authors
  1. Takahiro Ishikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shun Tamaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takanori Maruta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shigeru Shigeoka
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takahiro Ishikawa .

Editor information

Editors and Affiliations

  1. Department of Biological Sciences, University of Memphis, Memphis, Tennessee, USA

    Steven D. Schwartzbach

  2. Faculty of Agriculture, Kindai University, Nara, Japan

    Shigeru Shigeoka

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Ishikawa, T., Tamaki, S., Maruta, T., Shigeoka, S. (2017). Biochemistry and Physiology of Reactive Oxygen Species in Euglena . In: Schwartzbach, S., Shigeoka, S. (eds) Euglena: Biochemistry, Cell and Molecular Biology. Advances in Experimental Medicine and Biology, vol 979. Springer, Cham. https://doi.org/10.1007/978-3-319-54910-1_4

Download citation

Publish with us

Policies and ethics

Search

Navigation