Mitochondrial RNA Editing and Processing in Diplonemid Protists

  • Drahomíra Faktorová
  • Matus Valach
  • Binnypreet Kaur
  • Gertraud Burger
  • Julius LukešEmail author
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 34)


RNA editing and processing in the mitochondrion of Diplonema papillatum and other diplonemids are arguably the most complex processes of their kind described in any organelle so far. Prior to translation, each transcript has to be accurately trans-spliced from gene fragments encoded on different circular chromosomes. About half of the transcripts are massively edited by several types of substitution editing and addition of blocks of uridines. Comparative analysis of mitochondrial RNA processing among the three euglenozoan groups, diplonemids, kinetoplastids, and euglenids, highlights major differences between these lineages. Diplonemids remain poorly studied, yet they were recently shown to be extremely diverse and abundant in the ocean and hence are rapidly attracting increasing attention. It is therefore important to turn them into genetically tractable organisms, and we report here that they indeed have the potential to become such.



We thank Daria Tashyreva, Galina Prokopchuk, and Anzhelika Butenko (Institute of Parasitology) for sharing unpublished data. Support from the Grant Agency of University of South Bohemia (050/2016/P to BK), the Czech Grant Agency (15-21974S and 16-18699S to JL), the ERC CZ (LL1601 to JL), the Canadian Institutes of Health Research (CIHR, MOP 70309 to GB), and from the Gordon and Betty Moore Foundation (GBMF4983.01 to GB and JL) is kindly acknowledged.


  1. Abad MG, Long Y, Willcox A, Gott JM, Gray MW, Jackman JE (2011) A role for tRNA(his) guanylyltransferase (Thg1)-like proteins from Dictyostelium discoideum in mitochondrial 5′-tRNA editing. RNA 17:613–623PubMedPubMedCentralCrossRefGoogle Scholar
  2. Adl SM, Simpson AGB, Lane CE, Lukeš J, Bass D, Bowser SS, Brown MW, Burki F, Dunthorn M, Hampl V, Heiss A, Hoppenrath M, Lara E, Le Gall L, Lynn DH, McManus H, Mitchell EA, Mozley-Stanridge SE, Parfrey LW, Pawlowski J, Rueckert S, Shadwick L, Schoch CL, Smirnov A, Spiegel FW (2012) The revised classification of eukaryotes. J Eukaryot Microbiol 59:429–493PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adler BK, Harris ME, Bertrand KI, Hajduk SL (1991) Modification of Trypanosoma brucei mitochondrial rRNA by posttranscriptional 3′ polyuridine tail formation. Mol Cell Biol 11:5878–5884PubMedPubMedCentralCrossRefGoogle Scholar
  4. Alfonzo JD, Söll D (2009) Mitochondrial tRNA import—the challenge to understand has just begun. Biol Chem 390:717–722PubMedPubMedCentralCrossRefGoogle Scholar
  5. Alfonzo JD, Thiemann O, Simpson L (1997) The mechanism of U insertion/deletion RNA editing in kinetoplastid mitochondria. Nucleic Acids Res 25:3571–3579CrossRefGoogle Scholar
  6. Ammerman ML, Downey KM, Hashimi H, Fisk JC, Tomasello DL, Faktorová D, Kafková L, King T, Lukeš J, Read LR (2012) Architecture of the trypanosome RNA editing accessory complex, MRB1. Nucleic Acids Res 40:5637–5650PubMedPubMedCentralCrossRefGoogle Scholar
  7. Aphasizhev R, Aphasizheva I (2011) Uridine insertion/deletion editing in trypanosomes: a playground for RNA-guided information transfer. WIREs 2:669–685CrossRefGoogle Scholar
  8. Ban T, Zhu JK, Melcher K, Xu HE (2015) Structural mechanisms of RNA recognition: sequence-specific and non-specific RNA-binding proteins and the Cas9-RNA-DNA complex. Cell Mol Life Sci 72:1045–1058PubMedCrossRefGoogle Scholar
  9. Benne R, van den Burg J, Brakenhoff JP, Sloof P, van Boom JH, Tromp MC (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46:819–826CrossRefPubMedGoogle Scholar
  10. Breglia SA, Yubuki N, Hoppenrath M, Leander BS (2010) Ultrastructure and molecular phylogenetic position of a novel euglenozoan with extrusive episymbiotic bacteria: Bihospites bacati n. Gen. Et sp. (Symbiontida). BMC Microbiol 10:145PubMedPubMedCentralCrossRefGoogle Scholar
  11. Bundschuh R, Altmüller J, Becker C, Nürnberg P, Gott JM (2011) Complete characterization of the edited transcriptome of the mitochondrion of Physarum polycephalum using deep sequencing of RNA. Nucleic Acids Res 39:6044–6055PubMedPubMedCentralCrossRefGoogle Scholar
  12. Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19:709–716PubMedCrossRefGoogle Scholar
  13. Burger G, Gray MW, Forget L, Lang BF (2013) Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol Evol 5:418–438PubMedPubMedCentralCrossRefGoogle Scholar
  14. Burger G, Moreira S, Valach M (2016) Genes in hiding. Trends Genet 32:553–565PubMedCrossRefGoogle Scholar
  15. Calvo SE, Clauser KR, Mootha VK (2016) MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins. Nucleic Acids Res 44:D1251–D1257PubMedCrossRefGoogle Scholar
  16. Cavalier-Smith T (2016) Higher classification and phylogeny of Euglenozoa. Eur J Protistol 56:250–276PubMedCrossRefGoogle Scholar
  17. Chaput H, Wang Y, Morse D (2002) Polyadenylated transcripts containing random gene fragments are expressed in dinoflagellate mitochondria. Protist 153:111–122PubMedCrossRefGoogle Scholar
  18. Chen C, Frankhouser D, Bundschuh R (2012) Comparison of insertional RNA editing in Myxomycetes. PLoS Comput Biol 8:e1002400PubMedPubMedCentralCrossRefGoogle Scholar
  19. de Vargas C, Audic S, Henry N, Decelle J, Mahé F, Logares R, Lara E, Berney C, Le Bescot N, Probert I, Carmichael M, Poulain J, Romac S, Colin S, Aury J-M, Bittner L, Chaffron S, Dunthorn M, Engelen S, Flegontova O, Guidi L, Horák A, Jaillon O, Lima Mendez G, Lukeš J, Malviya S, Morard R, Mulot M, Scalco E, Siano R, Vincent F, Zingone A, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Acinas SG, Bork P, Bowler C, Gaill F, Gorsky G, Grimsley N, Hingcamp P, Iudicone D, Not F, Ogata H, Pesant S, Raes J, Sieracki M, Speich S, Stemmann L, Sunagawa S, Weissenbach J, Wincker P, Karsenti E, Boss E, Follows M, Karp-Boss L, Krzic U, Reynaud EG, Sardet C, Sullivan MB, Velayoudon D (2015) Eukaryotic plankton diversity in the sunlit global ocean. Science 348:1261605PubMedCrossRefGoogle Scholar
  20. Dejung M, Subota I, Bucerius F, Dindar G, Freiwald A, Engstler M, Boshart M, Butter F, Janzen CJ (2016) Quantitative proteomics uncovers novel factors involved in developmental differentiation of Trypanosoma brucei. PLoS Pathog 12:e1005439PubMedPubMedCentralCrossRefGoogle Scholar
  21. Desmond E, Brochier-Armanet C, Forterre P, Gribaldo S (2011) On the last common ancestor and early evolution of eukaryotes: reconstructing the history of mitochondrial ribosomes. Res Microbiol 162:53–70PubMedCrossRefGoogle Scholar
  22. Dixit S, Müller-McNicoll M, David V, Zarnack K, Ule J, Hashimi H, Lukeš J (2017) Differential binding of mitochondrial transcripts by MRB8170 and MRB4160 regulates distinct editing fates of mitochondrial mRNA in trypanosomes. MBio 8:e02288-16PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dobáková E, Flegontov P, Skalický T, Lukeš J (2015) Unexpectedly streamlined mitochondrial genome of the euglenozoan Euglena gracilis. Genome Biol Evol 7:3358–3367PubMedPubMedCentralCrossRefGoogle Scholar
  24. Edgcomb VP, Breglia SA, Yubuki N, Beaudoin D, Patterson DJ, Leander BS, Bernhard JM (2011) Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution. ISME J 5:231–243PubMedCrossRefGoogle Scholar
  25. Eloe EA, Shulse CN, Fadrosh DW, Williamson SJ, Allen EE, Bartlett DH (2011) Compositional differences in particle-associated and free-living microbial assemblages from an extreme deep-ocean environment. Environ Microbiol Rep 3:449–458PubMedCrossRefGoogle Scholar
  26. El-Sayed NM, Myler PJ, Blandin G, Berriman M, Crabtree J, Aggarwal G, Caler E, Renauld H, Worthey EA, Hertz-Fowler C, Ghedin E, Peacock C, Bartholomeu DC, Hass BJ, Tran A-N, Wortman JR, Alsmark UCM, Angiuoli S, Anupama A, Badger J, Bringaud F, Cadag E, Carlton JM, Cerqueira GC, Creasy T, Delcher AL, Djikeng A, Embley TM, Hauser C, Ivens AC, Kummerfeld SK, Pereira-Leal JB, Nilsoon D, Peterson J, Salzberg SL, Shallom J, Silva JC, Sundaram J, Westenberger S, White O, Melville SE, Donelson JE, Andersson B, Stuart KD, Hall N (2005) Comparative genomics of trypanosomatid parasitic protozoa. Science 309:404–409PubMedCrossRefGoogle Scholar
  27. Faktorová D, Dobáková E, Peña-Diaz P, Lukeš J (2016) From simple to supercomplex: mitochondrial genomes of euglenozoan protists. F1000 Res 5:392CrossRefGoogle Scholar
  28. Flegontov P, Gray MW, Burger G, Lukeš J (2011) Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa? Curr Genet 57:225–232PubMedCrossRefGoogle Scholar
  29. Flegontov P, Michálek J, Janouškovec J, Lai D-H, Jirků M, Hajdušková E, Tomčala A, Otto TD, Keeling PJ, Pain A, Oborník M, Lukeš J (2015) Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites. Mol Biol Evol 32:1115–1131PubMedCrossRefGoogle Scholar
  30. Flegontova O, Flegontov P, Malviya S, Audic S, Wincker P, de Vargas C, Bowler C, Lukeš J, Horák A (2016) Unexpected diversity and abundance of planktonic diplonemids in the world ocean. Curr Biol 26:3060–3065PubMedCrossRefGoogle Scholar
  31. Fu C-J, Sheikh S, Miao W, Andersson SGE, Baldauf SL (2014) Missing genes, multiple ORFs, and C-to-U type RNA editing in Acrasis kona (Heterolobosea, Discoba) mitochondrial DNA. Genome Biol Evol 6:2240–2257PubMedPubMedCentralCrossRefGoogle Scholar
  32. Gawryluk RMR, Chisholm KA, Pinto DM, Gray MW (2014) Compositional complexity of the mitochondrial proteome of a unicellular eukaryote (Acanthamoeba castellanii, supergroup Amoebozoa) rivals that of animals, fungi, and plants. J Proteome 109:400–416CrossRefGoogle Scholar
  33. Gawryluk RMR, del Campo J, Okamoto N, Strassert JFH, Lukeš J, Richards TA, Worden AZ, Santoro AE, Keeling PJ (2016) Morphological identification and single-cell genomics of marine diplonemids. Curr Biol 26:3053–3059PubMedCrossRefGoogle Scholar
  34. Gonzalez TN, Sidrauski C, Dörfler S, Walter P (1999) Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J 18:3119–3132PubMedPubMedCentralCrossRefGoogle Scholar
  35. Göringer HU (2012) ‘Gestalt,’ composition and function of the Trypanosoma brucei editosome. Annu Rev Microbiol 66:65–82PubMedCrossRefGoogle Scholar
  36. Gott JM, Parimi N, Bundschuh R (2005) Discovery of new genes and deletion editing in Physarum mitochondria enabled by a novel algorithm for finding edited mRNAs. Nucleic Acids Res 33:5063–5072PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gray MW (2012) Mitochondrial evolution. Cold Spring Harb Perspect Biol 4:a011403PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hudson AJ, Stark MR, Fast NM, Russell AG, Rader SD (2015) Splicing diversity revealed by reduced spliceosomes in C. merolae and other organisms. RNA Biol 12:1–8PubMedCrossRefGoogle Scholar
  39. Jackman JE, Gott JM, Gray MW (2012) Doing it in reverse: 3′-to-5′ polymerization by the Thg1 superfamily. RNA 18:886–899PubMedPubMedCentralCrossRefGoogle Scholar
  40. Jackson CJ, Waller RF (2013) A widespread and unusual RNA trans-splicing type in dinoflagellate mitochondria. PLoS One 8:e56777PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jackson CJ, Norman JE, Schnare MN, Gray MW, Keeling PJ, Waller RF (2007) Broad genomic and transcriptional analysis reveals a highly derived genome in dinoflagellate mitochondria. BMC Biol 5:41PubMedPubMedCentralCrossRefGoogle Scholar
  42. Karnkowska A, Vacek V, Zubáčová Z, Treitli SC, Petrželková R, Eme L, Novák L, Žárský V, Barlow LD, Herman EK, Soukal P, Hroudová M, Doležal P, Stairs CW, Roger AJ, Eliáš M, Dacks JB, Vlček Č, Hampl V (2016) A eukaryote without a mitochondrial organelle. Curr Biol 26:1274–1284PubMedCrossRefGoogle Scholar
  43. Kaur B, Valach M, Peña-Diaz P, Moreira S, Keeling PJ, Burger G, Lukeš J, Faktorová D (2018) Transformation of Diplonema papillatum, the type species of the highly diverse and abundant marine microeukaryotes Diplonemida (Euglenozoa). Environ Microbiol 20:1030–1040PubMedCrossRefGoogle Scholar
  44. Kiethega GN, Turcotte M, Burger G (2011) Evolutionary conserved cox1 trans-splicing without cis-motifs. Mol Biol Evol 28:2425–2458PubMedCrossRefGoogle Scholar
  45. Kiethega GN, Yan Y, Turcotte M, Burger G (2013) RNA-level unscrambling of fragmented genes in Diplonema mitochondria. RNA Biol 10:301–313PubMedPubMedCentralCrossRefGoogle Scholar
  46. Knoop V (2010) When you can’t trust the DNA: RNA editing changes transcript sequences. Cell Mol Life Sci 68:567–586PubMedCrossRefGoogle Scholar
  47. Kuai L, Fang F, Butler JS, Sherman F (2004) Polyadenylation of rRNA in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 101:8581–8586PubMedPubMedCentralCrossRefGoogle Scholar
  48. Laforest MJ, Roewer I, Lang BF (1997) Mitochondrial tRNAs in the lower fungus Spizellomyces punctatus: tRNA editing and UAG ‘stop’ codons recognized as leucine. Nucleic Acids Res 25:626–632PubMedPubMedCentralCrossRefGoogle Scholar
  49. Lara E, Moreira D, Vereshchaka A, López-García P (2009) Panoceanic distribution of new highly diverse clades of deep-sea diplonemids. Environ Microbiol 11:47–55PubMedCrossRefGoogle Scholar
  50. Lavrov DV, Adamski M, Chevaldonné P, Adamska M (2016) Extensive mitochondrial mRNA editing and unusual mitochondrial genome organization in calcaronean sponges. Curr Biol 26:86–92PubMedCrossRefGoogle Scholar
  51. Leander BS, Triemer RE, Farmer MA (2001) Character evolution in heterotrophic euglenids. Eur J Protistol 37:337–356CrossRefGoogle Scholar
  52. Lee WJ, Simpson AGB (2014) Morphological and molecular characterisation of Notosolenus urceolatus Larsen and Patterson 1990, a member of an understudied deepbranching euglenid group (petalomonads). J Eukaryot Microbiol 61:463–479PubMedCrossRefGoogle Scholar
  53. Leigh J, Lang BF (2004) Mitochondrial 3′ tRNA editing in the jakobid Seculamonas ecuadoriensis: a novel mechanism and implications for tRNA processing. RNA 10:615–621PubMedPubMedCentralCrossRefGoogle Scholar
  54. Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, Friedman N, Gnirke A, Regev A (2010) Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 7:709–715PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lin S, Zhang H, Spencer DF, Norman JE, Gray MW (2002) Widespread and extensive editing of mitochondrial mRNAs in dinoflagellates. J Mol Biol 320:727–739CrossRefPubMedGoogle Scholar
  56. Lithgow T, Schneider A (2010) Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc B Sci 365:799–817CrossRefGoogle Scholar
  57. López-García P, Rodríguez-Valera F, Pedrós-Alió C, Moreira D (2001) Unexpected diversity of small eukaryotes in deep-sea Antarctic plankton. Nature 409:603–607PubMedCrossRefGoogle Scholar
  58. López-García P, Vereshchaka A, Moreira D (2007) Eukaryotic diversity associated with carbonates and fluid seawater interface in Lost City hydrothermal field. Environ Microbiol 9:546–554PubMedCrossRefGoogle Scholar
  59. Lukeš J, Archibald JM, Keeling PJ, Doolittle WF, Gray MW (2011) How a neutral evolutionary ratchet can build cellular complexity. IUBMB Life 63:528–537CrossRefPubMedGoogle Scholar
  60. Lukeš J, Flegontova O, Horák A (2015) Diplonemids. Curr Biol 25:R702–R704PubMedCrossRefGoogle Scholar
  61. Maguire F, Richards TA (2014) Organelle evolution: a mosaic of ‘mitochondrial’ functions. Curr Biol 24:R518–R520PubMedCrossRefGoogle Scholar
  62. Mahendran R, Spottswood MR, Miller DL (1991) RNA editing by cytidine insertion in mitochondria of Physarum polycephalum. Nature 349:434–438CrossRefPubMedGoogle Scholar
  63. Manna S (2015) An overview of pentatricopeptide repeat proteins and their applications. Biochimie 113:93–99PubMedCrossRefGoogle Scholar
  64. Marande W, Burger G (2007) Mitochondrial DNA as a genomic jigsaw puzzle. Science 318:415PubMedCrossRefGoogle Scholar
  65. Marande W, Lukeš J, Burger G (2005) Unique mitochondrial genome structure in diplonemids, the sister group of kinetoplastids. Eukaryot Cell 4:1137–1146PubMedPubMedCentralCrossRefGoogle Scholar
  66. Maslov DA, Yasuhira S, Simpson L (1999) Phylogenetic affinities of Diplonema within the Euglenozoa as inferred from the SSU rRNA gene and partial COI protein sequences. Protist 150:33–42PubMedCrossRefGoogle Scholar
  67. Mohanty BK, Kushner SR (2011) Bacterial/archaeal/organellar polyadenylation. WIREs 2:256–276CrossRefGoogle Scholar
  68. Moreira S, Breton S, Burger G (2012) Unscrambling of genetic information at the RNA level. WIREs 3:213–228CrossRefGoogle Scholar
  69. Moreira S, Valach M, Aoulad-Aissa M, Otto C, Burger G (2016) Novel modes of RNA editing in mitochondria. Nucleic Acids Res 44:4907–4919PubMedPubMedCentralCrossRefGoogle Scholar
  70. Nishikura K (2016) A-to-I editing of coding and non-coding RNAs by ADARs. Nat Rev Mol Cell Biol 17:83–96CrossRefPubMedGoogle Scholar
  71. Okamoto N, Gawryluk RMR, del Campo J, Strassert JFH, Lukeš J, Richards TA, Worden AZ, Santoro AE, Keeling PJ (2018) Eupelagonema oceanica n. gen. & sp. and a revised diplonemid taxonomy. J Eukaryot Microbiol (in press)Google Scholar
  72. Ozsolak F, Milos PM (2011) RNA sequencing: advances, challenges and opportunities. Nat Rev Genet 12:87–98PubMedCrossRefGoogle Scholar
  73. Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A (2009) Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37:e123PubMedPubMedCentralCrossRefGoogle Scholar
  74. Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C, Bowser SS, Čepička I, Decelle J, Dunthorn M, Fiore-Donno A-M, Gile HG, Holzmann M, Jahn R, Jirků M, Keeling PJ, Kostka M, Kudryavtsev A, Lara E, Lukeš J, Mann GD, Mitchell ADE, Nitsche F, Romeralo M, Saunders WG, Simpson AGB, Smirnov VA, Spouge J, Stern FR, Stoeck T, Zimmermann J, Schindel D, de Vargas C (2012) CBOL Protist working group: barcoding eukaryotic richness beyond the animal, plant and fungal kingdoms. PLoS Biol 10:e1001419PubMedPubMedCentralCrossRefGoogle Scholar
  75. Popow J, Schleiffer A, Martinez J (2012) Diversity and roles of (t)RNA ligases. Cell Mol Life Sci 69:2657–2670PubMedPubMedCentralCrossRefGoogle Scholar
  76. Rammelt C, Rossmanith W (2016) Repairing tRNA termini: news from the 3′ end. RNA Biol 13:1182–1188PubMedPubMedCentralCrossRefGoogle Scholar
  77. Read LK, Lukeš J, Hashimi H (2016) Trypanosome RNA editing: the complexity of getting U in and taking U out. WIREs 7:33–51CrossRefGoogle Scholar
  78. Roy J, Faktorová D, Lukeš J, Burger G (2007) Unusual mitochondrial genome structures throughout the Euglenozoa. Protist 158:385–396PubMedCrossRefGoogle Scholar
  79. Rubio MAT, Pastar I, Gaston KW, Ragone FL, Janzen CJ, Cross GAM, Papavasiliou FN, Alfonzo JD (2007) An adenosine-to-inosine tRNA-editing enzyme that can perform C-to-U deamination of DNA. Proc Natl Acad Sci U S A 104:7821–7826PubMedPubMedCentralCrossRefGoogle Scholar
  80. Rüdinger M, Fritz-Laylin L, Polsakiewicz M, Knoop V (2011) Plant-type mitochondrial RNA editing in the protist Naegleria gruberi. RNA 17:2058–2062PubMedPubMedCentralCrossRefGoogle Scholar
  81. Salone V, Rüdinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, Szurek B, Small I, Knoop V, Lurin C (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett 581:4132–4138CrossRefPubMedGoogle Scholar
  82. Schnepf E (1994) Light and electron microscopical observations in Rhynchopus coscinodiscivorus spec. Nov., a colorless, phagotrophic Euglenozoon with concealed flagella. Arch Protistenkd 144:63–74CrossRefGoogle Scholar
  83. Segovia R, Pett W, Trewick S, Lavrov DV (2011) Extensive and evolutionarily persistent mitochondrial tRNA editing in velvet worms (phylum Onychophora). Mol Biol Evol 28:2873–2881PubMedCrossRefGoogle Scholar
  84. Shapiro TA, Englund PT (1995) The structure and replication of kinetoplast DNA. Annu Rev Microbiol 49:117–143PubMedCrossRefGoogle Scholar
  85. Shikanai T (2015) RNA editing in plants: machinery and flexibility of site recognition. Biochim Biophys Acta 1847:779–785CrossRefPubMedGoogle Scholar
  86. Škodová-Sveráková I, Verner Z, Skalický T, Votýpka J, Horváth A, Lukeš J (2015) Lineage-specific activities of a multipotent mitochondrion of trypanosomatid flagellates. Mol Microbiol 96:55–67PubMedCrossRefGoogle Scholar
  87. Slomovic S, Fremder E, Staals RH, Pruijn GJ, Schuster G (2010) Addition of poly(a) and poly(a)-rich tails during RNA degradation in the cytoplasm of human cells. Proc Natl Acad Sci U S A 107:7407–7412PubMedPubMedCentralCrossRefGoogle Scholar
  88. Smith DR, Keeling PJ (2015) Mitochondrial and plastid genome architecture: reoccurring themes, but significant differences at the extremes. Proc Natl Acad Sci U S A 112:10177–10184PubMedPubMedCentralCrossRefGoogle Scholar
  89. Spencer DF, Gray MW (2011) Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: fragmented genes in a seemingly fragmented genome. Mol Gen Genomics 285:19–31CrossRefGoogle Scholar
  90. Stahley MR, Strobel SA (2006) RNA splicing: group I intron crystal structures reveal the basis of splice site selection and metal ion catalysis. Curr Opin Struct Biol 16:319–326PubMedCrossRefGoogle Scholar
  91. Stuart K, Feagin JE (1992) Mitochondrial DNA of kinetoplastids. Int Rev Cytol 141:65–88PubMedCrossRefGoogle Scholar
  92. Sun T, Bentolila S, Hanson MR (2016) The unexpected diversity of plant organelle RNA editosomes. Trends Plant Sci 21:962–973CrossRefPubMedGoogle Scholar
  93. Szklarczyk R, Huynen MA (2010) Mosaic origin of the mitochondrial proteome. Proteomics 10:4012–4024PubMedCrossRefGoogle Scholar
  94. Takenaka M, Zehrmann A, Verbitskiy D, Härtel B, Brennicke A (2013) RNA editing in plants and its evolution. Annu Rev Genet 47:335–352CrossRefPubMedGoogle Scholar
  95. Tanaka N, Meineke B, Shuman S (2011) RtcB, a novel RNA ligase, can catalyze tRNA splicing and HAC1 mRNA splicing in vivo. J Biol Chem 286:30253–30257PubMedPubMedCentralCrossRefGoogle Scholar
  96. Tashyreva D, Prokopchuk G, Yabuki A, Kaur B, Faktorová D, Votýpka J, Kusaka C, Fujikura K, Shiratori T, Ishida K, Horák A, Lukeš J (2018) Phylogeny and morphology of diplonemids from the Sea of Japan. Protist 169:158–179PubMedCrossRefGoogle Scholar
  97. Tielens AGM, van Hellemond JJ (2009) Surprising variety in energy metabolism within Trypanosomatidae. Trends Parasitol 25:482–490PubMedCrossRefGoogle Scholar
  98. Triemer RE, Ott DW (1990) Ultrastructure of Diplonema ambulator Larsen & Patterson (Euglenozoa) and its relationship to Isonema. Eur J Protistol 25:316–320PubMedCrossRefGoogle Scholar
  99. Urbaniak MD, Martin DM, Ferguson MA (2013) Global quantitative SILAC phosphoproteomics reveals differential phosphorylation is widespread between the procyclic and bloodstream form lifecycle stages of Trypanosoma brucei. J Proteome Res 12:2233–2244PubMedPubMedCentralCrossRefGoogle Scholar
  100. Valach M, Moreira S, Kiethega GN, Burger G (2014) Trans splicing and RNA editing of LSU rRNA in Diplonema mitochondria. Nucleic Acids Res 42:2660–2672CrossRefPubMedGoogle Scholar
  101. Valach M, Moreira S, Faktorová D, Lukeš J, Burger G (2016) Post-transcriptional mending of gene sequences: looking under the hood of mitochondrial gene expression in diplonemids. RNA Biol 13:1204–1211PubMedPubMedCentralCrossRefGoogle Scholar
  102. Valach M, Moreira S, Hoffmann S, Stadler PF, Burger G (2017) Keeping it complicated: mitochondrial genome plasticity in diplonemids. Sci Rep 7:14166PubMedPubMedCentralCrossRefGoogle Scholar
  103. Vanfleteren JR, Vierstraete AR (1999) Insertional RNA editing in metazoan mitochondria: the cytochrome b gene in the nematode Teratocephalus lirellus. RNA 5:622–624PubMedPubMedCentralCrossRefGoogle Scholar
  104. Verner Z, Basu S, Benz C, Dixit S, Dobáková E, Faktorová D, Hashimi H, Horáková E, Huang Z, Paris Z, Pena-Diaz P, Ridlon L, Týč J, Wildridge D, Zíková A, Lukeš J (2015) Malleable mitochondrion of Trypanosoma brucei. Int Rev Cell Mol Biol 315:73–151PubMedCrossRefGoogle Scholar
  105. Visomirski-Robic LM, Gott JM (1997) Insertional editing of nascent mitochondrial RNAs in Physarum. Proc Natl Acad Sci U S A 94:4324–4329PubMedPubMedCentralCrossRefGoogle Scholar
  106. Vlcek Č, Marande W, Teijeiro S, Lukeš J, Burger G (2011) Gene fragments scattered across a multi-partite mitochondrial genome. Nucleic Acids Res 39:979–988PubMedCrossRefGoogle Scholar
  107. Wahlstedt H, Ohman M (2011) Site-selective versus promiscuous A-to-I editing. WIREs 2:761–771CrossRefGoogle Scholar
  108. Wheeler RJ, Gull K, Gluenz E (2012) Detailed interrogation of trypanosome cell biology via differential organelle staining and automated image analysis. BMC Biol 10:1PubMedPubMedCentralCrossRefGoogle Scholar
  109. Yabuki A, Tame A (2015) Phylogeny and reclassification of Hemistasia phaeocysticola (Scherffel) Elbrachter & Schnepf, 1996. J Eukaryot Microbiol 62:426–429PubMedCrossRefGoogle Scholar
  110. Yabuki A, Tanifuji G, Kusaka C, Takishita K, Fujikura K (2016) Hyper-eccentric structural genes in the mitochondrial genome of the algal parasite Hemistasia phaeocysticola. Genome Biol Evol:8, 2870–2878Google Scholar
  111. Yang J, Harding T, Kamikawa R, Simpson AGB, Roger AJ (2017) Mitochondrial genome evolution and a novel RNA editing system in deep-branching heteroloboseids. Genome Biol Evol 9:1161–1174PubMedPubMedCentralCrossRefGoogle Scholar
  112. Yokobori S, Pääbo S (1995) Transfer RNA editing in land snail mitochondria. Proc Natl Acad Sci U S A 92:10432–10435PubMedPubMedCentralCrossRefGoogle Scholar
  113. Yubuki N, Edgcomb VP, Bernhard JM, Leander BS (2009) Ultrastructure and molecular phylogeny of Calkinsia aureus: cellular identity of a novel clade of deep-sea euglenozoans with epibiotic bacteria. BMC Microbiol 27:16CrossRefGoogle Scholar
  114. Yubuki N, Simpson AG, Leander BS (2013) Reconstruction of the feeding apparatus in Postgaardi mariagerensis provides evidence for character evolution within the Symbiontida (Euglenozoa). Eur J Protistol 49:32–39PubMedCrossRefGoogle Scholar
  115. Zhao C, Pyle AM (2017) Structural insights into the mechanism of group II intron splicing. Trends Biochem Sci 42:470–482PubMedPubMedCentralCrossRefGoogle Scholar
  116. Zíková A, Verner Z, Nenarokova A, Michels PAM, Lukeš J (2017) A paradigm shift: the mitoproteomes of procyclic and bloodstream Trypanosoma brucei are comparably complex. PLoS Pathog 13:e1006679PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zimorski V, Ku C, Martin W, Gould SB (2014) Endosymbiotic theory for organelle origins. Curr Opin Microbiol 22:38–48PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Drahomíra Faktorová
    • 1
  • Matus Valach
    • 2
  • Binnypreet Kaur
    • 1
  • Gertraud Burger
    • 2
  • Julius Lukeš
    • 1
    Email author
  1. 1.Institute of Parasitology, Biology Centre and Faculty of Sciences, University of South BohemiaČeské BudějoviceCzech Republic
  2. 2.Department of Biochemistry and Robert-CedergrenCentre for Bioinformatics and Genomics, Université de MontréalMontrealCanada

Personalised recommendations