Mitochondria are double membrane organelles of endosymbiotic origin, best known for constituting the centre of energetics of a eukaryotic cell. They contain their own mitochondrial genome, which as a consequence of gradual reduction during evolution typically contains less than two dozens of genes. In this review, we highlight the extremely diverse architecture of mitochondrial genomes and mechanisms of gene expression between the three sister groups constituting the phylum Euglenozoa - Euglenida, Diplonemea and Kinetoplastea. The earliest diverging euglenids possess a simplified mitochondrial genome and a conventional gene expression, whereas both are highly complex in the two other groups. The expression of their mitochondrial-encoded proteins requires extensive post-transcriptional modifications guided by complex protein machineries and multiple small RNA molecules. Moreover, the least studied diplonemids, which have been recently discovered as a highly abundant component of the world ocean plankton, possess one of the most complicated mitochondrial genome organisations known to date.

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic; Canadian Institute for Adavanced Research Toronto Ontario Canada

Institute of Parasitology Biology Centre Czech Academy of Sciences České Budějovice Czech Republic; Departments of Biochemistry and Genetics Faculty of Natural Sciences Comenius Universtity Bratislava Slovakia

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Adl SM, Simpson AG, Lane CE, et al. : The revised classification of eukaryotes. J Eukaryot Microbiol. 2012;59(5):429–93. 10.1111/j.1550-7408.2012.00644.x PubMed DOI PMC

Lukeš J, Skalický T, Týč J, et al. : Evolution of parasitism in kinetoplastid flagellates. Mol Biochem Parasitol. 2014;195(2):115–22. 10.1016/j.molbiopara.2014.05.007 PubMed DOI

Hampl V, Hug L, Leigh JW, et al. : Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups". Proc Natl Acad Sci U S A. 2009;106(10):3859–64. 10.1073/pnas.0807880106 PubMed DOI PMC

de Vargas C, Audic S, Henry N, et al. : Ocean plankton. Eukaryotic plankton diversity in the sunlit ocean. Science. 2015;348(6237):1261605. 10.1126/science.1261605 PubMed DOI

Lukeš J, Flegontova O, Horák A: Diplonemids. Curr Biol. 2015;25(16):R702–4. 10.1016/j.cub.2015.04.052 PubMed DOI

Tielens AG, van Hellemond JJ: Surprising variety in energy metabolism within Trypanosomatidae. Trends Parasitol. 2009;25(10):482–90. 10.1016/j.pt.2009.07.007 PubMed DOI

Zíková A, Hampl V, Paris Z, et al. : Aerobic mitochondria of parasitic protists: Diverse genomes and complex functions. Mol Biochem Parasitol. 2016; pii: S0166-6851(16)30015-9. 10.1016/j.molbiopara.2016.02.007 PubMed DOI

Marande W, Lukes J, Burger G: Unique mitochondrial genome structure in diplonemids, the sister group of kinetoplastids. Eukaryot Cell. 2005;4(6):1137–46. 10.1128/EC.4.6.1137-1146.2005 PubMed DOI PMC

Smith DR, Keeling PJ: Mitochondrial and plastid genome architecture: Reoccurring themes, but significant differences at the extremes. Proc Natl Acad Sci U S A. 2015;112(33):10177–84. 10.1073/pnas.1422049112 PubMed DOI PMC

Pawlowski J, Audic S, Adl S, et al. : CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol. 2012;10(11):e1001419. 10.1371/journal.pbio.1001419 PubMed DOI PMC

Gray MW: Diversity and evolution of mitochondrial RNA editing systems. IUBMB Life. 2003;55(4–5):227–33. 10.1080/1521654031000119425 PubMed DOI

Smith DR: The past, present and future of mitochondrial genomics: have we sequenced enough mtDNAs? Brief Funct Genomics. 2016;15(1):47–54. 10.1093/bfgp/elv027 PubMed DOI PMC

Flegontov P, Michálek J, Janouškovec J, et al. : Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites. Mol Biol Evol. 2015;32(5):1115–31. 10.1093/molbev/msv021 PubMed DOI

Burger G, Gray MW, Forget L, et al. : Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol Evol. 2013;5(2):418–38. 10.1093/gbe/evt008 PubMed DOI PMC

Roy J, Faktorová D, Lukes J, et al. : Unusual mitochondrial genome structures throughout the Euglenozoa. Protist. 2007;158(3):385–96. 10.1016/j.protis.2007.03.002 PubMed DOI

Lukes J, Guilbride DL, Votýpka J, et al. : Kinetoplast DNA network: evolution of an improbable structure. Eukaryot Cell. 2002;1(4):495–502. 10.1128/EC.1.4.495-502.2002 PubMed DOI PMC

Jensen RE, Englund PT: Network news: the replication of kinetoplast DNA. Annu Rev Microbiol. 2012;66:473–91. 10.1146/annurev-micro-092611-150057 PubMed DOI

Povelones ML: Beyond replication: division and segregation of mitochondrial DNA in kinetoplastids. Mol Biochem Parasitol. 2014;196(1):53–60. 10.1016/j.molbiopara.2014.03.008 PubMed DOI

Verner Z, Basu S, Benz C, et al. : Malleable mitochondrion of Trypanosoma brucei. Int Rev Cell Mol Biol. 2015;315:73–151. 10.1016/bs.ircmb.2014.11.001 PubMed DOI

Liu B, Liu Y, Motyka SA, et al. : Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol. 2005;21(8):363–9. 10.1016/j.pt.2005.06.008 PubMed DOI

Borst P, Fase-Fowler F, Weijers PJ, et al. : Kinetoplast DNA from Trypanosoma vivax and T. congolense. Mol Biochem Parasitol. 1985;15(2):129–42. 10.1016/0166-6851(85)90114-8 PubMed DOI

Sloof P, de Haan A, Eier W, et al. : The nucleotide sequence of the variable region in Trypanosoma brucei completes the sequence analysis of the maxicircle component of mitochondrial kinetoplast DNA. Mol Biochem Parasitol. 1992;56(2):289–99. 10.1016/0166-6851(92)90178-M PubMed DOI

Shapiro TA, Englund PT: The structure and replication of kinetoplast DNA. Annu Rev Microbiol. 1995;49:117–43. 10.1146/annurev.mi.49.100195.001001 PubMed DOI

Benne R, De Vries BF, Van den Burg J, et al. : The nucleotide sequence of a segment of Trypanosoma brucei mitochondrial maxi-circle DNA that contains the gene for apocytochrome b and some unusual unassigned reading frames. Nucleic Acids Res. 1983;11(20):6925–41. 10.1093/nar/11.20.6925 PubMed DOI PMC

Simpson L, Neckelmann N, de la Cruz VF, et al. : Comparison of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei at the level of nucleotide sequence. J Biol Chem. 1987;262(13):6182–96. PubMed

Koslowsky D, Sun Y, Hindenach J, et al. : The insect-phase gRNA transcriptome in Trypanosoma brucei. Nucleic Acids Res. 2014;42(3):1873–86. 10.1093/nar/gkt973 PubMed DOI PMC

Aphasizhev R, Aphasizheva I: Mitochondrial RNA editing in trypanosomes: small RNAs in control. Biochimie. 2014;100:125–31. 10.1016/j.biochi.2014.01.003 PubMed DOI PMC

Read LK, Lukeš J, Hashimi H: Trypanosome RNA editing: the complexity of getting U in and taking U out. Wiley Interdiscip Rev RNA. 2016;7(1):33–51. 10.1002/wrna.1313 PubMed DOI PMC

Alfonzo JD, Blanc V, Estévez AM, et al. : C to U editing of the anticodon of imported mitochondrial tRNA Trp allows decoding of the UGA stop codon in Leishmania tarentolae. EMBO J. 1999;18(24):7056–62. 10.1093/emboj/18.24.7056 PubMed DOI PMC

Alfonzo JD, Söll D: Mitochondrial tRNA import--the challenge to understand has just begun. Biol Chem. 2009;390(8):717–22. 10.1515/BC.2009.101 PubMed DOI PMC

Vlcek C, Marande W, Teijeiro S, et al. : Systematically fragmented genes in a multipartite mitochondrial genome. Nucleic Acids Res. 2011;39(3):979–88. 10.1093/nar/gkq883 PubMed DOI PMC

Kiethega GN, Yan Y, Turcotte M, et al. : RNA-level unscrambling of fragmented genes in Diplonema mitochondria. RNA Biol. 2013;10(2):301–13. 10.4161/rna.23340 PubMed DOI PMC

Marande W, Burger G: Mitochondrial DNA as a genomic jigsaw puzzle. Science. 2007;318(5849):415. 10.1126/science.1148033 PubMed DOI

Valach M, Burger G, Gray MW, et al. : Widespread occurrence of organelle genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res. 2014;42(22):13764–77. 10.1093/nar/gku1266 PubMed DOI PMC

Moreira S, Valach M, Aoulad-Aissa M, et al. : Novel modes of RNA editing in mitochondria. Nucleic Acids Res. 2016;44(10):4907–19. 10.1093/nar/gkw188 PubMed DOI PMC

Spencer DF, Gray MW: Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: fragmented genes in a seemingly fragmented genome. Mol Genet Genomics. 2011;285(1):19–31. 10.1007/s00438-010-0585-9 PubMed DOI

Tessier LH, van der Speck H, Gualberto JM, et al. : The cox1 gene from Euglena gracilis: a protist mitochondrial gene without introns and genetic code modifications. Curr Genet. 1997;31(3):208–13. 10.1007/s002940050197 PubMed DOI

Dobáková E, Flegontov P, Skalický T, et al. : Unexpectedly Streamlined Mitochondrial Genome of the Euglenozoan Euglena gracilis. Genome Biol Evol. 2015;7(12):3358–67. 10.1093/gbe/evv229 PubMed DOI PMC

Lukeš J, Archibald JM, Keeling PJ, et al. : How a neutral evolutionary ratchet can build cellular complexity. IUBMB Life. 2011;63(7):528–37. 10.1002/iub.489 PubMed DOI

Zíková A, Panigrahi AK, Dalley RA, et al. : Trypanosoma brucei mitochondrial ribosomes: affinity purification and component identification by mass spectrometry. Mol Cell Proteomics. 2008;7(7):1286–96. 10.1074/mcp.M700490-MCP200 PubMed DOI PMC

Ridlon L, Škodová I, Pan S, et al. : The importance of the 45 S ribosomal small subunit-related complex for mitochondrial translation in Trypanosoma brucei. J Biol Chem. 2013;288(46):32963–78. 10.1074/jbc.M113.501874 PubMed DOI PMC

Horvath A, Kingan TG, Maslov DA: Detection of the mitochondrially encoded cytochrome c oxidase subunit I in the trypanosomatid protozoan Leishmania tarentolae. Evidence for translation of unedited mRNA in the kinetoplast. J Biol Chem. 2000;275(22):17160–5. 10.1074/jbc.M907246199 PubMed DOI

Škodová-Sveráková I, Horváth A, Maslov DA: Identification of the mitochondrially encoded subunit 6 of F 1F O ATPase in Trypanosoma brucei . Mol Biochem Parasitol. 2015;201(2):135–8. 10.1016/j.molbiopara.2015.08.002 PubMed DOI PMC

Cech TR: RNA editing: world's smallest introns? Cell. 1991;64(4):667–9. 10.1016/0092-8674(91)90494-J PubMed DOI

Flegontov P, Gray MW, Burger G, et al. : Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa? Curr Genet. 2011;57(4):225–32. 10.1007/s00294-011-0340-8 PubMed DOI

Gray MW, Lukes J, Archibald JM, et al. : Cell biology. Irremediable complexity? Science. 2010;330(6006):920–1. 10.1126/science.1198594 PubMed DOI

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