Genes encoding enzymes of the tetrapyrrole biosynthetic pathway were searched within Euglena gracilis EST databases and 454 genome reads and their 5' end regions were sequenced when not available. Phylogenetic analyses and protein localization predictions support the hypothesis concerning the presence of two separated tetrapyrrole pathways in E. gracilis. One of these pathways resembles the heme synthesis in primarily heterotrophic eukaryotes and was presumably present in the host cell prior to secondary endosymbiosis with a green alga. The second pathway is similar to the plastid-localized tetrapyrrole syntheses in plants and photosynthetic algae. It appears to be localized to the secondary plastid, presumably derived from an algal endosymbiont and probably serves only for the production of plastidial heme and chlorophyll. Thus, E. gracilis represents an evolutionary intermediate in a metabolic transformation of a primary heterotroph to a photoautotroph through secondary endosymbiosis. We propose here that the tetrapyrrole pathway serves as a highly informative marker for the evolution of plastids and plays a crucial role in the loss of plastids.

Department of Molecular Biology of Protists Biology Centre of the Academy of Sciences of the Czech Republic Institute of Parasitology České Budějovice Czech Republic

Zobrazit více v PubMed

Camadro JM, Chambon H, Jolles J, Labbe P. Purification and properties of coproporphyrinogen oxidase from the yeast Saccharomyces cerevisiae. Eur J Biochem. 1986;156:579–587. PubMed

Cook JR. Irreversible plastid loss in Euglena gracilis under physiological conditions. Plant Physiol. 1974;53:284–290. PubMed PMC

Corriveau JL, Beale SI. Influence of gabaculine on growth, chlorophyll synthesis, and δ-aminolevulinic acid synthase activity in Euglena gracilis. Plant Sci. 1986;45:9–17.

Dailey TA, Woodruff JH, Dailey HA. Examination of mitochondrial protein targeting of haem synthetic enzymes: in vivo identification of three functional haem-responsive motifs in 5-aminolaevulinate synthase. Biochem J. 2005;386:381–386. PubMed PMC

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

Ferreira GC, Andrew TL, Karr SW, Dailey HA. Organization of the terminal two enzymes of the heme biosynthetic pathway. Orientation of protoporphyrinogen oxidase and evidence for a membrane complex. J Biol Chem. 1988;263:3835–3839. PubMed

Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999;41:95–98.

Iida K, Kajiwara M. Carbon source dependence of the ratio of δ-aminolevulinic acid biosynthesis via the C5 and shemin pathways in Euglena gracilis (Euglenophyceae) J Phycol. 2008;44:292–298. PubMed

Iida K, Mimura I, Kajiwara M. Evaluation of two biosynthetic pathways to δ-aminolevulinic acid in Euglena gracilis. Eur J Biochem. 2002;269:291–297. PubMed

Ikeda S, Takata N. Deoxyribonuclease II purified from Euglena gracilis SM-ZK, a chloroplast-lacking mutant: comparison with porcine spleen deoxyribonuclease II. Comp Biochem Phys B Biochem Mol Biol. 2002;131:519–525. PubMed

Juknat AA, Dornemann D, Senger H. Different porphobilinogenases in cytoplasm and isolated-chloroplasts from light-grown Euglena gracilis Z. Z Naturforsch C. 1989;44:81–84.

Katoh K, Toh H. Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform. 2008;9:286–298. PubMed

Koch M, et al. Crystal structure of protoporphyrinogen IX oxidase: a key enzyme in haem and chlorophyll biosynthesis. EMBO J. 2004;23:1720–1728. PubMed PMC

Kořený L, Lukeš J, Oborník M. Evolution of the haem synthetic pathway in kinetoplastid flagellates: an essential pathway that is not essential after all? Int J Parasitol. 2010;40:149–156. PubMed

Lartillot N, Philippe H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol. 2004;21:1095–1109. PubMed

Masoumi A, et al. Complex formation between protoporphyrinogen IX oxidase and ferrochelatase during haem biosynthesis in Thermosynechococcus elongatus. Microbiology. 2008;154:3707–3714. PubMed

Mather W, Vaidya AB. Mitochondria in malaria and related parasites: ancient, diverse and streamlined. J Bioenerg Biomembr. 2008;40:425–433. PubMed

Mayer SM, Beale SI. δ-aminolevulinic acid biosynthesis from glutamate in Euglena gracilis. Plant Physiol. 1991;97:1094–1102. PubMed PMC

Mayer SM, Beale SI, Weinstein JD. Enzymatic conversion of glutamate to δ-aminolevulinic acid in soluble extracts of Euglena gracilis. J Biol Chem. 1987;262:12541–12549. PubMed

Nagaraj VA, Arumugam R, Prasad D, Rangarajan PN, Padmanaban G. Protoporphyrinogen IX oxidase from Plasmodium falciparum is anaerobic and is localized to the mitochondrion. Mol Biochem Parasitol. 2010;174:44–52. PubMed

Nagaraj VA, Prasad D, Arumugam R, Rangarajan PN, Padmanaban G. Characterization of coproporphyrinogen III oxidase in Plasmodium falciparum cytosol. Parasitol Int. 2010;59:121–127. PubMed

Nagaraj VA, Prasad D, Rangarajan PN, Padmanaban G. Mitochondrial localization of functional ferrochelatase from Plasmodium falciparum. Mol Biochem Parasitol. 2009;168:109–112. PubMed

Nicolas P. Sensitivity of Euglena gracilis to chloroplast-inhibiting antibiotics, and properties of antibiotic-resistant mutants. Plant Sci Lett. 1981;22:309–316.

Oborník M, Green BR. Mosaic origin of the heme biosynthesis pathway in photosynthetic eukaryotes. Mol Biol Evol. 2005;22:2343–2353. PubMed

Oborník M, Janouškovec J, Chrudimský T, Lukeš J. Evolution of the apicoplast and its hosts: from heterotrophy to autotrophy and back again. Int J Parasitol. 2009;39:1–12. PubMed

Ohki Y, Hasegawa K, Musashi A, Tsubo Y. Loss of chloroplastic DNA in a Euglena mutant during growth in darkness. Arch Microbiol. 1984;139:147–150.

Okazaki T, Kurumaya K, Sagae Y, Kajiwara M. Studies on the biosynthesis of corrinoids and porphyrinoids. IV. Biosynthesis of chlorophyll in Euglena gracilis. Chem Pharm Bull. 1990;38:3303–3307. PubMed

Osafune T, Schiff JA. W10BSmL, a mutant of Euglena gracilis var. bacillaris lacking plastids. Exp Cell Res. 1983;148:530–536. PubMed

Panek H, O'Brian MR. A whole genome view of prokaryotic haem biosynthesis. Microbiology. 2002;148:2273–2282. PubMed

Petříček M, Petříčková K, Havlíček L, Felsberg J. Occurrence of two 5-aminolevulinate biosynthetic pathways in Streptomyces nodosus subsp. asukaensis is linked with the production of asukamycin. J Bacteriol. 2006;188:5113–5123. PubMed PMC

Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ. The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts. Mol Biol Evol. 2007;24:54–62. PubMed

Rossetti MV, Juknat AA, Battle AMD. Soluble and particulate porphobilinogen-deaminase from dark-grown Euglena gracilis. Z Naturforsch C. 1989;44:578–580.

Rossetti MV, et al. Porphyrin biosynthesis in Euglena gracilis-V. Soluble and particulate PBG-ASE. Comp Biochem Phys B. 1986;85:451–458.

Russell GK, Draffan AG. Light-induced enzyme formation in a chlorophyll-less mutant of Euglena gracilis. Plant Physiol. 1978;62:678–682. PubMed PMC

Sato S, Clough B, Coates L, Wilson RJM. Enzymes for heme biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum. Protist. 2004;155:117–125. PubMed

Schulze JO, Schubert WD, Moser J, Jahn D, Heinz DW. Evolutionary relationship between initial enzymes of tetrapyrrole biosynthesis. J Mol Biol. 2006;358:1212–1220. PubMed

Shashidara LS, Smith AG. Expression and subcellular location of the tetrapyrrole synthesis enzyme porphobilinogen deaminase in light-grown Euglena gracilis and three nonchlorophyllous cell lines. Proc Natl Acad Sci U S A. 1991;88:63–67. PubMed PMC

Sobotka R, Tichý M, Wilde A, Hunter CN. Functional assignments for the C-terminal domains of the ferrochelatase from Synechocystis PCC 6803: the CAB domain plays a regulatory role and region II is essential for catalysis. Plant Physiol. 2010 doi:10.1104/pp.110.167528. PubMed PMC

Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22:2688–2690. PubMed

Stange-Thomann N, Thomann H-U, Lloyd AJ, Lyman H, Söll D. A point mutation in Euglena gracilis chloroplast tRNA(Glu) uncouples protein and chlorophyll biosynthesis. Proc Natl Acad Sci U S A. 1994;91:7947–7951. PubMed PMC

Templeton TJ, et al. A genome-sequence survey for Ascogregarina taiwanensis supports evolutionary affiliation but metabolic diversity between a gregarine and Cryptosporidium. Mol Biol Evol. 2010;27:235–248. PubMed PMC

van Dooren GG, Stimmler LM, McFadden GI. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol Rev. 2006;30:596–630. PubMed

Weinstein JD, Beale SI. Separate physiological roles and subcellular compartments for two tetrapyrrole biosynthetic pathways in Euglena gracilis. J Biol Chem. 1983;258:6799–6807. PubMed

Wu B. Heme biosynthetic pathway in apicomplexan parasites. 2006. [dissertation]. University of Pennsylvania. Available from ProQuest. Publication number 3246256.

Localization of heme biosynthesis in the diatom Phaeodactylum tricornutum and differential expression of multi-copy enzymes

Heterotrophic euglenid Rhabdomonas costata resembles its phototrophic relatives in many aspects of molecular and cell biology

Using Diatom and Apicomplexan Models to Study the Heme Pathway of Chromera velia

Enigmatic Evolutionary History of Porphobilinogen Deaminase in Eukaryotic Phototrophs

The Cryptic Plastid of Euglena longa Defines a New Type of Nonphotosynthetic Plastid Organelle

Peculiar features of the plastids of the colourless alga Euglena longa and photosynthetic euglenophytes unveiled by transcriptome analyses

Evolution of the Tetrapyrrole Biosynthetic Pathway in Secondary Algae: Conservation, Redundancy and Replacement

Heme pathway evolution in kinetoplastid protists

Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites

Make it, take it, or leave it: heme metabolism of parasites

Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites

Zobrazit více v PubMed

GENBANK
JF292577, JF292578, JF292579, JF292580, JF292581, JF292582, JF292583, JF292584, JF292585, JF292586, JF292587