Catalase and Ascorbate Peroxidase in Euglenozoan Protists
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
LM2015042
Czech Ministry of Education
LM2015085
CERIT-Scientific Cloud
LL1601
ERC CZ
18-15962S
Grant Agency of Czech Republic
20-07186S
Grant Agency of Czech Republic
OPVVV/0000759
European Regional Funds
1/0781/19
Grant Agency of the Slovak Ministry of Education and the Academy of Sciences
1/0387/17
Grant Agency of the Slovak Ministry of Education and the Academy of Sciences
APVV-0286-12
Slovak Research and Development Agency
PubMed
32344595
PubMed Central
PMC7237987
DOI
10.3390/pathogens9040317
PII: pathogens9040317
Knihovny.cz E-zdroje
- Klíčová slova
- Euglenozoa, ascorbate peroxidase, catalase, enzymatic activity, phylogeny,
- Publikační typ
- časopisecké články MeSH
In this work, we studied the biochemical properties and evolutionary histories of catalase (CAT) and ascorbate peroxidase (APX), two central enzymes of reactive oxygen species detoxification, across the highly diverse clade Eugenozoa. This clade encompasses free-living phototrophic and heterotrophic flagellates, as well as obligate parasites of insects, vertebrates, and plants. We present evidence of several independent acquisitions of CAT by horizontal gene transfers and evolutionary novelties associated with the APX presence. We posit that Euglenozoa recruit these detoxifying enzymes for specific molecular tasks, such as photosynthesis in euglenids and membrane-bound peroxidase activity in kinetoplastids and some diplonemids.
Faculty of Natural Sciences Comenius University 841 04 Bratislava Slovakia
Faculty of Science Charles University BIOCEV 128 00 Prague Czech Republic
Faculty of Sciences University of South Bohemia 370 05 České Budějovice Czech Republic
Life Science Research Centre Faculty of Science University of Ostrava 710 00 Ostrava Czech Republic
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Bilinski T. Oxygen toxicity and microbial evolution. Biosystems. 1991;24:305–312. doi: 10.1016/0303-2647(91)90049-Q. PubMed DOI
Lü J.M., Lin P.H., Yao Q., Chen C. Chemical and molecular mechanisms of antioxidants: Experimental approaches and model systems. J. Cell Mol. Med. 2010;14:840–860. doi: 10.1111/j.1582-4934.2009.00897.x. PubMed DOI PMC
Gill S.S., Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010;48:909–930. doi: 10.1016/j.plaphy.2010.08.016. PubMed DOI
Avery S.V. Molecular targets of oxidative stress. Biochem. J. 2011;434:201–210. doi: 10.1042/BJ20101695. PubMed DOI
Apel K., Hirt H. Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 2004;55:373–399. doi: 10.1146/annurev.arplant.55.031903.141701. PubMed DOI
Asada K., Takahashi M. In: Production and Scavenging of Active Oxygen in Chloroplasts. Photoinhibition D.J., Kyle C.B., Arntzen C.J., editors. Elsevier; Amsterdam, The Netherlands: 1987. pp. 227–287.
Bowler C., Montagu M.V., Inze D. Superoxide dismutase and stress tolerance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1992;43:83–116. doi: 10.1146/annurev.pp.43.060192.000503. DOI
Willekens H., Chamnongpol S., Davey M., Schraudner M., Langebartels C., Van Montagu M., Inze D., Van Camp W. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 1997;16:4806–4816. doi: 10.1093/emboj/16.16.4806. PubMed DOI PMC
Takeda T., Yoshimura K., Yoshii M., Kanahoshi H., Miyasaka H., Shigeoka S. Molecular characterization and physiological role of ascorbate peroxidase from halotolerant Chlamydomonas sp. W80 strain. Arch. Biochem. Biophys. 2000;376:82–90. doi: 10.1006/abbi.1999.1564. PubMed DOI
Wilkinson S.R., Obado S.O., Mauricio I.L., Kelly J.M. Trypanosoma cruzi expresses a plant-like ascorbate-dependent hemoperoxidase localized to the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA. 2002;99:13453–13458. doi: 10.1073/pnas.202422899. PubMed DOI PMC
Shigeoka S., Nakano Y., Kitaoka S. Metabolism of hydrogen peroxide in Euglena gracilis Z by L-ascorbic acid peroxidase. Biochem. J. 1980;186:377–380. doi: 10.1042/bj1860377. PubMed DOI PMC
Caverzan A., Passaia G., Rosa S.B., Ribeiro C.W., Lazzarotto F., Margis-Pinheiro M. Plant responses to stresses: Role of ascorbate peroxidase in the antioxidant protection. Genet. Mol. Biol. 2012;35(Suppl. 4):1011–1019. doi: 10.1590/S1415-47572012000600016. PubMed DOI PMC
Vlasits J., Jakopitsch C., Schwanninger M., Holubar P., Obinger C. Hydrogen peroxide oxidation by catalase-peroxidase follows a non-scrambling mechanism. FEBS Lett. 2007;581:320–324. doi: 10.1016/j.febslet.2006.12.037. PubMed DOI
Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci. 2002;7:405–410. doi: 10.1016/S1360-1385(02)02312-9. PubMed DOI
De Marco A., Roubelakis-Angelakis K.A. The complexity of enzymic control of hydrogen peroxide concentration may affect the regeneration potential of plant protoplasts. Plant Physiol. 1996;110:137–145. doi: 10.1104/pp.110.1.137. PubMed DOI PMC
Shigeoka S., Ishikawa T., Tamoi M., Miyagawa Y., Takeda T., Yabuta Y., Yoshimura K. Regulation and function of ascorbate peroxidase isoenzymes. J. Exp. Bot. 2002;53:1305–1319. doi: 10.1093/jexbot/53.372.1305. PubMed DOI
Teixeira F.K., Menezes-Benavente L., Margis R., Margis-Pinheiro M. Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: Inferences from the rice genome. J. Mol. Evol. 2004;59:761–770. doi: 10.1007/s00239-004-2666-z. PubMed DOI
Teixeira F.K., Menezes-Benavente L., Galvao V.C., Margis R., Margis-Pinheiro M. Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments. Planta. 2006;224:300–314. doi: 10.1007/s00425-005-0214-8. PubMed DOI
Mittler R., Vanderauwera S., Gollery M., Van Breusegem F. Reactive oxygen gene network of plants. Trends Plant Sci. 2004;9:490–498. doi: 10.1016/j.tplants.2004.08.009. PubMed DOI
Glorieux C., Calderon P.B. Catalase, a remarkable enzyme: Targeting the oldest antioxidant enzyme to find a new cancer treatment approach. Biol. Chem. 2017;398:1095–1108. doi: 10.1515/hsz-2017-0131. PubMed DOI
Fairlamb A.H., Blackburn P., Ulrich P., Chait B.T., Cerami A. Trypanothione: A novel bis(glutathionyl)spermidine cofactor for glutathione reductase in trypanosomatids. Science. 1985;227:1485–1487. doi: 10.1126/science.3883489. PubMed DOI
Carnieri E.G., Moreno S.N., Docampo R. Trypanothione-dependent peroxide metabolism in Trypanosoma cruzi different stages. Mol. Biochem. Parasitol. 1993;61:79–86. doi: 10.1016/0166-6851(93)90160-Y. PubMed DOI
Adak S., Pal S. Ascorbate peroxidase acts as a novel determiner of redox homeostasis in Leishmania. Antioxid. Redox Signal. 2013;19:746–754. doi: 10.1089/ars.2012.4745. PubMed DOI
Montrichard F., Le Guen F., Laval-Martin D.L., Davioud-Charvet E. Evidence for the co-existence of glutathione reductase and trypanothione reductase in the non-trypanosomatid Euglenozoa: Euglena gracilis Z. FEBS Lett. 1999;442:29–33. doi: 10.1016/S0014-5793(98)01606-8. PubMed DOI
Zimorski V., Rauch C., van Hellemond J.J., Tielens A.G.M., Martin W.F. The mitochondrion of Euglena gracilis. Adv. Exp. Med. Biol. 2017;979:19–37. PubMed
Butenko A., Opperdoes F.R., Flegontova O., Horak A., Hampl V., Keeling P., Gawryluk R.M.R., Tikhonenkov D., Flegontov P., Lukeš J. Evolution of metabolic capabilities and molecular features of diplonemids, kinetoplastids, and euglenids. BMC Biol. 2020;18:23. doi: 10.1186/s12915-020-0754-1. PubMed DOI PMC
Mittler R., Herr E.H., Orvar B.L., van Camp W., Willekens H., Inze D., Ellis B.E. Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl. Acad. Sci. USA. 1999;96:14165–14170. doi: 10.1073/pnas.96.24.14165. PubMed DOI PMC
Opperdoes F.R., Szikora J.P. In silico prediction of the glycosomal enzymes of Leishmania major and trypanosomes. Mol. Biochem. Parasitol. 2006;147:193–206. doi: 10.1016/j.molbiopara.2006.02.010. PubMed DOI
Bianchi C., Kostygov A.Y., Kraeva N., Záhonová K., Horáková E., Sobotka R., Lukeš J., Yurchenko V. An enigmatic catalase of Blastocrithidia. Mol. Biochem. Parasitol. 2019;232:111199. doi: 10.1016/j.molbiopara.2019.111199. PubMed DOI
Kraeva N., Horáková E., Kostygov A., Kořený L., Butenko A., Yurchenko V., Lukeš J. Catalase in Leishmaniinae: With me or against me? Infect. Genet. Evol. 2017;50:121–127. doi: 10.1016/j.meegid.2016.06.054. PubMed DOI
Schott E.J., Di Lella S., Bachvaroff T.R., Amzel L.M., Vasta G.R. Lacking catalase, a protistan parasite draws on its photosynthetic ancestry to complete an antioxidant repertoire with ascorbate peroxidase. BMC Evol. Biol. 2019;19:146. doi: 10.1186/s12862-019-1465-5. PubMed DOI PMC
Adl S.M., Bass D., Lane C.E., Lukeš J., Schoch C.L., Smirnov A., Agatha S., Berney C., Brown M.W., Burki F., et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 2019;66:4–119. doi: 10.1111/jeu.12691. PubMed DOI PMC
Lukeš J., Skalický T., Týč J., Votýpka J., Yurchenko V. Evolution of parasitism in kinetoplastid flagellates. Mol. Biochem. Parasitol. 2014;195:115–122. doi: 10.1016/j.molbiopara.2014.05.007. PubMed DOI
Adak S., Datta A.K. Leishmania major encodes an unusual peroxidase that is a close homologue of plant ascorbate peroxidase: A novel role of the transmembrane domain. Biochem. J. 2005;390:465–474. doi: 10.1042/BJ20050311. PubMed DOI PMC
Mittler R., Zilinskas B.A. Purification and characterization of pea cytosolic ascorbate peroxidase. Plant Physiol. 1991;97:962–968. doi: 10.1104/pp.97.3.962. PubMed DOI PMC
Wada K., Tada T., Nakamura Y., Ishikawa T., Yabuta Y., Yoshimura K., Shigeoka S., Nishimura K. Crystal structure of chloroplastic ascorbate peroxidase from tobacco plants and structural insights into its instability. J. Biochem. 2003;134:239–244. doi: 10.1093/jb/mvg136. PubMed DOI
Pitsch N.T., Witsch B., Baier M. Comparison of the chloroplast peroxidase system in the chlorophyte Chlamydomonas reinhardtii, the bryophyte Physcomitrella patens, the lycophyte Selaginella moellendorffii and the seed plant Arabidopsis thaliana. BMC Plant Biol. 2010;10:133. doi: 10.1186/1471-2229-10-133. PubMed DOI PMC
Opperdoes F.R., Butenko A., Flegontov P., Yurchenko V., Lukeš J. Comparative metabolism of free-living Bodo saltans and parasitic trypanosomatids. J. Eukaryot. Microbiol. 2016;63:657–678. doi: 10.1111/jeu.12315. PubMed DOI
Horáková E., Faktorová D., Kraeva N., Kaur B., Van Den Abbeele J., Yurchenko V., Lukeš J. Catalase compromises the development of the insect and mammalian stages of Trypanosoma brucei. FEBS J. 2020;287:964–977. doi: 10.1111/febs.15083. PubMed DOI
Ishemgulova A., Butenko A., Kortišová L., Boucinha C., Grybchuk-Ieremenko A., Morelli K.A., Tesařová M., Kraeva N., Grybchuk D., Pánek T., et al. Molecular mechanisms of thermal resistance of the insect trypanosomatid Crithidia thermophila. PLoS ONE. 2017;12:e0174165. doi: 10.1371/journal.pone.0174165. PubMed DOI PMC
Kraeva N., Butenko A., Hlaváčová J., Kostygov A., Myškova J., Grybchuk D., Leštinová T., Votýpka J., Volf P., Opperdoes F., et al. Leptomonas seymouri: Adaptations to the dixenous life cycle analyzed by genome sequencing, transcriptome profiling and co-infection with Leishmania donovani. PLoS Pathog. 2015;11:e1005127. doi: 10.1371/journal.ppat.1005127. PubMed DOI PMC
Záhonová K., Füssy Z., Birčák E., Novák-Vanclová A.M.G., Klimeš V., Vesteg M., Krajčovič J., Oborník M., Eliáš M. Peculiar features of the plastids of the colourless alga Euglena longa and photosynthetic euglenophytes unveiled by transcriptome analyses. Sci. Rep. 2018;8:17012. doi: 10.1038/s41598-018-35389-1. PubMed DOI PMC
Zámocký M., Gasselhuber B., Furtmüller P.G., Obinger C. Turning points in the evolution of peroxidase-catalase superfamily: Molecular phylogeny of hybrid heme peroxidases. Cell Mol. Life Sci. 2014;71:4681–4696. doi: 10.1007/s00018-014-1643-y. PubMed DOI PMC
Asada K. Ascorbate peroxidase—A hydrogen peroxide-scavenging enzyme in plants. Physiol. Plant. 1992;85:235–241. doi: 10.1111/j.1399-3054.1992.tb04728.x. DOI
Mittra B., Cortez M., Haydock A., Ramasamy G., Myler P.J., Andrews N.W. Iron uptake controls the generation of Leishmania infective forms through regulation of ROS levels. J. Exp. Med. 2013;210:401–416. doi: 10.1084/jem.20121368. PubMed DOI PMC
Khan Y.A., Andrews N.W., Mittra B. ROS regulate differentiation of visceralizing Leishmania species into the virulent amastigote form. Parasitol. Open. 2018;4:e19. doi: 10.1017/pao.2018.15. PubMed DOI PMC
Opperdoes F.R., Nohýnková E., Van Schaftingen E., Lambeir A.M., Veenhuis M., Van Roy J. Demonstration of glycosomes (microbodies) in the Bodonid flagellate Trypanoplasma borelli (Protozoa, Kinetoplastida) Mol. Biochem. Parasitol. 1988;30:155–163. doi: 10.1016/0166-6851(88)90108-9. PubMed DOI
Ishikawa T., Tajima N., Nishikawa H., Gao Y., Rapolu M., Shibata H., Sawa Y., Shigeoka S. Euglena gracilis ascorbate peroxidase forms an intramolecular dimeric structure: Its unique molecular characterization. Biochem. J. 2010;426:125–134. doi: 10.1042/BJ20091406. PubMed DOI
Novák Vanclová A.M.G., Zoltner M., Kelly S., Soukal P., Záhonová K., Füssy Z., Ebenezer T.E., Lacová Dobáková E., Eliáš M., Lukeš J., et al. Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid. New Phytol. 2020;225:1578–1592. doi: 10.1111/nph.16237. PubMed DOI
Lazzarotto F., Teixeira F.K., Rosa S.B., Dunand C., Fernandes C.L., Fontenele Ade V., Silveira J.A., Verli H., Margis R., Margis-Pinheiro M. Ascorbate peroxidase-related (APx-R) is a new heme-containing protein functionally associated with ascorbate peroxidase but evolutionarily divergent. New Phytol. 2011;191:234–250. doi: 10.1111/j.1469-8137.2011.03659.x. PubMed DOI
Koussevitzky S., Suzuki N., Huntington S., Armijo L., Sha W., Cortes D., Shulaev V., Mittler R. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem. 2008;283:34197–34203. doi: 10.1074/jbc.M806337200. PubMed DOI PMC
Kostygov A.Y., Yurchenko V. Revised classification of the subfamily Leishmaniinae (Trypanosomatidae) Folia Parasitol. 2017;64:020. doi: 10.14411/fp.2017.020. PubMed DOI
Ajithkumar I.P., Panneerselvam R. ROS scavenging system, osmotic maintenance, pigment and growth status of Panicum sumatrense roth under drought stress. Cell Biochem. Biophys. 2014;68:587–595. doi: 10.1007/s12013-013-9746-x. PubMed DOI
Maslov D.A., Opperdoes F.R., Kostygov A.Y., Hashimi H., Lukeš J., Yurchenko V. Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitology. 2019;146:1–27. doi: 10.1017/S0031182018000951. PubMed DOI
Záhonová K., Füssy Z., Oborník M., Eliáš M., Yurchenko V. RuBisCO in non-photosynthetic alga Euglena longa: Divergent features, transcriptomic analysis and regulation of complex formation. PLoS ONE. 2016;11:e0158790. PubMed PMC
Ebenezer T.E., Zoltner M., Burrell A., Nenarokova A., Novák Vanclová A.M.G., Prasad B., Soukal P., Santana-Molina C., O’Neill E., Nankissoor N.N., et al. Transcriptome, proteome and draft genome of Euglena gracilis. BMC Biol. 2019;17:11. doi: 10.1186/s12915-019-0626-8. PubMed DOI PMC
Smircich P., Eastman G., Bispo S., Duhagon M.A., Guerra-Slompo E.P., Garat B., Goldenberg S., Munroe D.J., Dallagiovanna B., Holetz F., et al. Ribosome profiling reveals translation control as a key mechanism generating differential gene expression in Trypanosoma cruzi. BMC Genom. 2015;16:443. doi: 10.1186/s12864-015-1563-8. PubMed DOI PMC
Parsons M., Myler P.J. Illuminating parasite protein production by ribosome profiling. Trends Parasitol. 2016;32:446–457. doi: 10.1016/j.pt.2016.03.005. PubMed DOI PMC
Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–3402. doi: 10.1093/nar/25.17.3389. PubMed DOI PMC
Savelli B., Li Q., Webber M., Jemmat A.M., Robitaille A., Zamocky M., Mathe C., Dunand C. RedoxiBase: A database for ROS homeostasis regulated proteins. Redox Biol. 2019;26:101247. doi: 10.1016/j.redox.2019.101247. PubMed DOI PMC
Benson D.A., Cavanaugh M., Clark K., Karsch-Mizrachi I., Ostell J., Pruitt K.D., Sayers E.W. GenBank. Nucleic Acids Res. 2018;46:D41–D47. doi: 10.1093/nar/gkx1094. PubMed DOI PMC
Jones P., Binns D., Chang H.Y., Fraser M., Li W., McAnulla C., McWilliam H., Maslen J., Mitchell A., Nuka G., et al. InterProScan 5: Genome-scale protein function classification. Bioinformatics. 2014;30:1236–1240. doi: 10.1093/bioinformatics/btu031. PubMed DOI PMC
Steinegger M., Soding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 2017;35:1026–1028. doi: 10.1038/nbt.3988. PubMed DOI
Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Capella-Gutiérrez S., Silla-Martinez J.M., Gabaldon T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–1973. doi: 10.1093/bioinformatics/btp348. PubMed DOI PMC
Wang H.C., Minh B.Q., Susko E., Roger A.J. Modeling site heterogeneity with posterior mean site frequency profiles accelerates accurate phylogenomic estimation. Syst. Biol. 2018;67:216–235. doi: 10.1093/sysbio/syx068. PubMed DOI
Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC
Hiller K., Grote A., Scheer M., Munch R., Jahn D. PrediSi: Prediction of signal peptides and their cleavage positions. Nucleic Acids Res. 2004;32:W375–W379. doi: 10.1093/nar/gkh378. PubMed DOI PMC
Kume K., Amagasa T., Hashimoto T., Kitagawa H. NommPred: Prediction of mitochondrial and mitochondrion-related organelle proteins of nonmodel organisms. Evol. Bioinform. Online. 2018;14:1176934318819835. doi: 10.1177/1176934318819835. PubMed DOI PMC
Almagro Armenteros J.J., Salvatore M., Emanuelsson O., Winther O., von Heijne G., Elofsson A., Nielsen H. Detecting sequence signals in targeting peptides using deep learning. Life Sci. Alliance. 2019;2:e201900429. doi: 10.26508/lsa.201900429. PubMed DOI PMC
Blum T., Briesemeister S., Kohlbacher O. MultiLoc2: Integrating phylogeny and Gene Ontology terms improves subcellular protein localization prediction. BMC Bioinform. 2009;10:274. doi: 10.1186/1471-2105-10-274. PubMed DOI PMC
Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 2001;305:567–580. doi: 10.1006/jmbi.2000.4315. PubMed DOI
Käll L., Krogh A., Sonnhammer E.L. Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server. Nucleic Acids Res. 2007;35:W429–W432. doi: 10.1093/nar/gkm256. PubMed DOI PMC
Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC
Škodová-Sveráková I., Prokopchuk G., Peña-Diaz P., Záhonová K., Moos M., Horváth A., Šimek P., Lukeš J. Unique dynamics of paramylon storage in the marine euglenozoan Diplonema papillatum. Protist. 2020;171:125717. doi: 10.1016/j.protis.2020.125717. PubMed DOI
Tashyreva D., Prokopchuk G., Votýpka J., Yabuki A., Horák A., Lukeš J. Life cycle, ultrastructure, and phylogeny of new diplonemids and their endosymbiotic bacteria. mBio. 2018;9:e02447–e17. doi: 10.1128/mBio.02447-17. PubMed DOI PMC
Yurchenko V., Kostygov A., Havlová J., Grybchuk-Ieremenko A., Ševčíková T., Lukeš J., Ševčík J., Votýpka J. Diversity of trypanosomatids in cockroaches and the description of Herpetomonas tarakana sp. n. J. Eukaryot. Microbiol. 2016;63:198–209. doi: 10.1111/jeu.12268. PubMed DOI
Changmai P., Horáková E., Long S., Černotíková-Stříbrná E., McDonald L.M., Bontempi E.J., Lukeš J. Both human ferredoxins equally efficiently rescue ferredoxin deficiency in Trypanosoma brucei. Mol. Microbiol. 2013;89:135–151. doi: 10.1111/mmi.12264. PubMed DOI
Hutner S.H., Zahalsky A.C., Aronson S.A., Baker H., Frank O. Culture media for Euglena gracilis. In: Prescott D.M., editor. Methods in Cell Physiology. Academic Press; New York, NY, USA: London, UK: 1966. pp. 217–228.
Cramer M., Myers J. Growth and photosynthetic characteristics of Euglena gracilis. Arch. Mikrobiol. 1952;17:384–402. doi: 10.1007/BF00410835. DOI
Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI
Monteiro G., Horta B.B., Pimenta D.C., Augusto O., Netto L.E. Reduction of 1-Cys peroxiredoxins by ascorbate changes the thiol-specific antioxidant paradigm, revealing another function of vitamin C. Proc. Natl. Acad. Sci. USA. 2007;104:4886–4891. doi: 10.1073/pnas.0700481104. PubMed DOI PMC
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