1932

Abstract

Apicomplexa are known to contain greatly reduced organellar genomes. Their mitochondrial genome carries only three protein-coding genes, and their plastid genome is reduced to a 35-kb-long circle. The discovery of coral-endosymbiotic algae and , which share a common ancestry with Apicomplexa, provided an opportunity to study possibly ancestral forms of organellar genomes, a unique glimpse into the evolutionary history of apicomplexan parasites. The structurally similar mitochondrial genomes of and differ in gene content, which is reflected in the composition of their respiratory chains. Thus, lacks respiratory complexes I and III, whereas and apicomplexan parasites are missing only complex I. Plastid genomes differ substantially between these algae, particularly in structure: The plastid genome is a linear, 120-kb molecule with large and divergent genes, whereas the plastid genome of is a highly compact circle that is only 85 kb long but nonetheless contains more genes than that of . It appears that organellar genomes have already been reduced in free-living phototrophic ancestors of apicomplexan parasites, and such reduction is not associated with parasitism.

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2015-10-15
2024-04-29
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Literature Cited

  1. Adl SM, Simpson AG, Lane CE, Lukeš J, Bass D. 1.  et al. 2012. The revised classification of eukaryotes. J. Euk. Microbiol. 59:429–93 [Google Scholar]
  2. Barbrook AC, Howe CJ. 2.  2000. Minicircular plastid DNA in the dinoflagellate Amphidinium operculatum. Mol. Gen. Genet. 263:152–58 [Google Scholar]
  3. Bína D, Gardian Z, Herbstová M, Kotabová E, Koník P. 3.  et al. 2014. Novel type of red-shifted chlorophyll a antenna complex from Chromera velia: II. Biochemistry and spectroscopy. Biochim. Biophys. Acta Bioenerg. 1837:802–10 [Google Scholar]
  4. Brouard JS, Otis C, Lemieux C, Turmel M. 4.  2010. The exceptionally large chloroplast genome of the green alga Floydiella terrestris illuminates the evolutionary history of the Chlorophyceae. Genome Biol. Evol. 2:240–56 [Google Scholar]
  5. Brunk CF, Lee LC, Tran AB, Li J. 5.  2003. Complete sequence of the mitochondrial genome of Tetrahymena thermophila and comparative methods for identifying highly divergent genes. Nucleic Acids Res. 31:1673–82 [Google Scholar]
  6. Burger G, Gray MW, Forget L, Lang BF. 6.  2013. Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol. Evol. 5:418–38 [Google Scholar]
  7. Burger G, Zhu Y, Littlejohn TG, Greenwood SJ, Schnare MN. 7.  et al. 2000. Complete sequence of the mitochondrial genome of Tetrahymena pyriformis and comparison with Paramecium aurelia mitochondrial DNA. J. Mol. Biol. 297:365–80 [Google Scholar]
  8. Cavalier-Smith T, Chao EE. 8.  2004. Protalveolate phylogeny and systematics and the origins of Sporozoa and dinoflagellates (phylum Myzozoa nom. nov.). Eur. J. Protistol. 40:185–212 [Google Scholar]
  9. Cumbo VR, Baird AH, Moore RB, Negri AP, Neilan BA. 9.  et al. 2013. Chromera velia is endosymbiotic in larvae of the reef corals Acropora digifera and A. tenuis. Protist 164:237–44 [Google Scholar]
  10. Dang Y, Green BR. 10.  2009. Substitutional editing of Heterocapsa triquetra chloroplast transcripts and a folding model for its divergent chloroplast 16S rRNA. Gene 442:73–80 [Google Scholar]
  11. de Graaf RM, Ricard G, van Alen TA, Duarte I, Dutilh BE. 11.  et al. 2011. The organellar genome and metabolic potential of the hydrogen-producing mitochondrion of Nyctotherus ovalis. Mol. Biol. Evol. 28:2379–91 [Google Scholar]
  12. De Koning AP, Keeling PJ. 12.  2006. The complete plastid genome sequence of the parasitic green alga Helicosporidium sp. is highly reduced and structured. BMC Biol. 4:12 [Google Scholar]
  13. Dorrell RG, Drew J, Nisbet RER, Howe CL. 13.  2014. Evolution of chloroplast transcript processing in Plasmodium and its chromerid algal relatives. PLOS Genet 10:e1004008 [Google Scholar]
  14. Durchan M, Kesan G, Šlouf V, Fuciman M, Staleva H. 14.  et al. 2014. Highly efficient energy transfer from a carbonyl carotenoid to chlorophyll a in the main light harvesting complex of Chromera velia. Biochim. Biophys. Acta Bioenerg. 1837:1748–55 [Google Scholar]
  15. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M. 15.  et al. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLOS Biol. 4:e286 [Google Scholar]
  16. Esseiva CA, Naguleswaran A, Hemphill A, Schneider A. 16.  2004. Mitochondrial tRNA import in Toxoplasma gondii. J. Biol. Chem. 279:42363–68 [Google Scholar]
  17. Feagin JE, Harrell MI, Lee JC, Coe KJ, Sands BH. 17.  et al. 2012. The fragmented mitochondrial ribosomal RNAs of Plasmodium falciparum. PLOS ONE 7:e38320 [Google Scholar]
  18. Feagin JE, Mericle BL, Werner E, Morris M. 18.  1997. Identification of additional rRNA fragments encoded by the Plasmodium falciparum 6 kb element. Nucleic Acid Res. 25:438–46 [Google Scholar]
  19. Flegontov P, Lukeš J. 19.  2012. Mitochondrial genomes of photosynthetic euglenids and alveolates. Adv. Bot. Res. 63:127–53 [Google Scholar]
  20. Flegontov P, Michálek J, Janouškovec J, Lai D-H, Jirků M. 20.  et al. 2015. Divergent mitochondrial respiratory chains in phototrophic relatives of apicomplexan parasites. Mol. Biol. Evol. 32:1115–31 [Google Scholar]
  21. Gabrielsen TM, Minge MA, Espelund M, Tooming-Klunderud A, Patil V. 21.  et al. 2011. Genome of a tertiary dinoflagellate plastid. PLOS ONE 6:e19132 [Google Scholar]
  22. Gile GH, Slamovits CH. 22.  2014. Transcriptomic analysis reveals evidence for a cryptic plastid in the colpodellid Voromonas pontica, a close relative of chromerids and apicomplexan parasites. PLOS ONE 9:e96258 [Google Scholar]
  23. Ginger ML, Fritz-Laylin LK, Fulton C, Cande WZ, Dawson SC. 23.  2010. Intermediary metabolism in protists: a sequence-based view of facultative anaerobic metabolism in evolutionarily diverse eukaryotes. Protist 161:642–71 [Google Scholar]
  24. Green BR. 24.  2004. The chloroplast genome of dinoflagellates—a reduced instruction set?. Protist 155:23–31 [Google Scholar]
  25. Gockel G, Hachtel W. 25.  2000. Complete gene map of the plastid genome of the non-photosynthetic euglenoid flagellate Astasia longa. Protist 151:347–51 [Google Scholar]
  26. Gould SB, Waller RR, McFadden GI. 26.  2008. Plastid evolution. Annu. Rev. Plant Biol. 59:491–517 [Google Scholar]
  27. Guo TJ, Weatherby K, Carter D, Šlapeta J. 27.  2010. Effect of nutrient concentration and salinity on immotile-motile transformation of Chromera velia. J. Euk. Microbiol. 57:444–46 [Google Scholar]
  28. Hallick RB, Hong L, Drager RG, Favreau MR, Monfort A. 28.  et al. 1993. Complete sequence of Euglena gracilis chloroplast DNA. Nucleic Acids Res. 21:3537–44 [Google Scholar]
  29. Hino A, Hirai M, Tanaka TQ, Watanabe Y, Matsuoka H, Kita K. 29.  2012. Critical roles of the mitochondrial complex II in oocyst formation of rodent malaria parasite Plasmodium berghei. J. Biochem. 152:259–68 [Google Scholar]
  30. Jackson CJ, Gornik SG, Waller RF. 30.  2012. The mitochondrial genome and transcriptome of the basal dinoflagellate Hematodinium sp.: character evolution within the highly derived mitochondrial genomes of dinoflagellates. Genome Biol. Evol. 4:59–72 [Google Scholar]
  31. Janouškovec J, Horák A, Oborník M, Lukeš J, Keeling PJ. 31.  2010. A common red algal origin of the apicomplexan, dinoflagellate and heterokont plastids. PNAS 107:10949–54 [Google Scholar]
  32. Janouškovec J, Sobotka R, Lai D-H, Flegontov P, Koník P. 32.  et al. 2013. Split photosystem protein, linear-mapping topology and growth of structural complexity in the plastid genome of Chromera velia. Mol. Biol. Evol. 30:2447–62 [Google Scholar]
  33. Janouškovec J, Tikhonenkov DV, Mikhailov KV, Simdyanov TG, Aleoshin VV. 33.  et al. 2013. Colponemids represent multiple ancient alveolate lineages. Curr. Biol. 23:2546–52 [Google Scholar]
  34. Jiroutová K, Kořený L, Bowler C, Oborník M. 34.  2010. A gene in the process of endosymbiotic transfer. PLOS ONE 5:e13234 [Google Scholar]
  35. Kamikawa R, Nishimura H, Sako Y. 35.  2009. Analysis of the mitochondrial genome, transcripts, and electron transport activity in the dinoflagellate Alexandrium catenella (Gonyaulacales, Dinophyceae). Phycol. Res. 57:1–11 [Google Scholar]
  36. Keeling PJ. 36.  2004. Diversity and evolutionary history of plastids and their hosts. Am. J. Bot. 91:1481–93 [Google Scholar]
  37. Keeling PJ. 37.  2008. Bridge over troublesome plastids. Nature 451:896–97 [Google Scholar]
  38. Keeling PJ. 38.  2013. The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu. Rev. Plant Biol. 64:583–607 [Google Scholar]
  39. Keithly JS, Langreth SG, Buttle KF, Mannella CA. 39.  2005. Electron tomographic and ultrastructural analysis of the Cryptosporidium parvum relict mitochondrion, its associated membranes, and organelles. J. Eukaryot. Microbiol. 52:132–40 [Google Scholar]
  40. Kořený L, Oborník M, Lukeš J. 40.  2013. Make it, take it or leave it: heme metabolism of parasites. PLOS Pathog. 9:e1003088 [Google Scholar]
  41. Kořený L, Sobotka R, Janouškovec J, Keeling PJ, Oborník M. 41.  2011. Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant Cell 23:3454–62 [Google Scholar]
  42. Kotabová E, Jarešová J, Kaňa R, Sobotka R, Bína D, Prášil O. 42.  2014. Novel type of red shifted chlorophyll antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems. Biochim. Biophys. Acta Bioenerg. 1837:734–43 [Google Scholar]
  43. Kotabová E, Kaňa R, Jarešová J, Prášil O. 43.  2011. Non-photochemical fluorescence quenching in Chromera velia is enabled by fast violaxanthin de-epoxidation. FEBS Lett. 585:1941–45 [Google Scholar]
  44. Lang-Unnasch N, Aiello DP. 44.  1999. Sequence evidence for an altered genetic code in the Neospora caninum plastid. Int. J. Parasitol. 29:1557–62 [Google Scholar]
  45. Lin RQ, Qiu LL, Liu GH, Wu XY, Weng YB. 45.  et al. 2011. Characterization of the complete mitochondrial genomes of five Eimeria species from domestic chickens. Gene 480:28–33 [Google Scholar]
  46. Lin S, Zhang H, Gray MW. 46.  2008. RNA editing in dinoflagellates and its implications for the evolutionary history of the editing machinery. RNA and DNA Editing: Molecular Mechanisms and Their Integration into Biological Systems HC Smith 280–309 Hoboken, NJ: Wiley [Google Scholar]
  47. Maguire F, Richards TA. 47.  2014. Organelle evolution: a mosaic of “mitochondrial” functions. Curr. Biol. 24:R518 [Google Scholar]
  48. Mann M, Hoppenz P, Jakob T, Weisheit W, Mittag M. 48.  et al. 2014. Unusual features of the high light acclimation of Chromera velia. Photosynth. Res. 122:159–69 [Google Scholar]
  49. Marcet-Houben M, Marceddu G, Gabaldón T. 49.  2009. Phylogenomics of the oxidative phosphorylation in fungi reveals extensive gene duplication followed by functional divergence. BMC Evol. Biol. 9:295 [Google Scholar]
  50. Masuda I, Matsuzaki M, Kita K. 50.  2010. Extensive frameshift at all AGG and CCC codons in the mitochondrial cytochrome c oxidase subunit 1 gene of Perkinsus marinus (Alveolata; Dinoflagellata). Nucleic Acids Res. 38:6186–94 [Google Scholar]
  51. McFadden GI. 51.  2014. Origin and evolution of plastids and photosynthesis in eukaryotes. Cold Spring Harb. Persp. Biol. 6:a016105 [Google Scholar]
  52. McFadden GI, Reith ME, Munholland J, Lang-Unnasch N. 52.  1996. Plastid in human parasites. Nature 381:482 [Google Scholar]
  53. Moore RB, Oborník M, Janouškovec J, Chrudimský T, Vancová M. 53.  et al. 2008. A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451:959–63 [Google Scholar]
  54. Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C. 54.  et al. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76:444–95 [Google Scholar]
  55. Nash EA, Nisbet RER, Barbrook AC, Howe CJ. 55.  2008. Dinoflagellates: a mitochondrial genome all at sea. Trends Genet. 24:328–35 [Google Scholar]
  56. Oborník M, Janouškovec J, Chrudimský T, Lukeš J. 56.  2009. Evolution of the apicoplast and its hosts: from heterotrophy to autotrophy and back again. Int. J. Parasitol. 39:1–12 [Google Scholar]
  57. Oborník M, Lukeš J. 57.  2013. Cell biology of chromerids, the autotrophic relatives to apicomplexan parasites. Int. Rev. Cell. Mol. Biol. 306:333–69 [Google Scholar]
  58. Oborník M, Modrý D, Lukeš M, Černotíková-Stříbrná E, Cihlář J. 58.  et al. 2012. Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist 163:306–23 [Google Scholar]
  59. Oborník M, Vancová M, Lai D-H, Janouškovec J, Keeling PJ, Lukeš J. 59.  2011. Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of Apicomplexa, Chromera velia. Protist 162:115–30 [Google Scholar]
  60. Pan H, Šlapeta J, Carter D, Chen M. 60.  2012. Phylogenetic analysis of the light harvesting systems in Chromera velia. Photosynth. Res. 111:19–28 [Google Scholar]
  61. Pan H, Šlapeta J, Carter D, Chen M. 61.  2013. Isolation of complete chloroplasts from Chromera velia—the photosynthetic relative of apicomplexan parasites. Photosynthesis Research for Food, Fuel and Future T Kuang, C Lu, L Zhang 436–39 Adv. Top. Sci. Technol. China Hangzhou, China: Zhejiang Univ. Press [Google Scholar]
  62. Petersen J, Ludewig A-K, Michael V, Bunk B, Jarek M. 62.  et al. 2014. Chromera velia, endosymbioses and the rhodoplex hypothesis—plastid evolution in cryptophytes, alveolates, stramenopiles, and haptophytes (CASH lineages). Genome Biol. Evol. 6:666–84 [Google Scholar]
  63. Porcel BM, Denoeud F, Opperdoes F, Noel B, Madoui M-A. 63.  et al. 2014. The streamlined genome of Phytomonas spp. relative to human pathogenic kinetoplastids reveals a parasite tailored for plants. PLOS Genet. 10:e1004007 [Google Scholar]
  64. Quigg A, Kotabová E, Jarešová J, Kaňa R, Šetlík J. 64.  et al. 2012. Photosynthesis in Chromera velia represents a simple system with high efficiency. PLOS ONE 7:e47036 [Google Scholar]
  65. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ. 65.  et al. 2004. Metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2:203–16 [Google Scholar]
  66. Robledo JAF, Caler E, Matsuzaki M, Keeling PJ, Shanmugam D. 66.  et al. 2011. The search for the missing link: a relic plastid in Perkinsus?. Int. J. Parasitol. 41:1217–29 [Google Scholar]
  67. Scharff LB, Koop HU. 67.  2006. Linear molecules of tobacco ptDNA end at known replication origins and additional loci. Plant Mol. Biol. 62:4–5 [Google Scholar]
  68. Seeber F, Limenitakis J, Soldati-Favre D. 68.  2008. Apicomplexan mitochondrial metabolism: a story of gains, losses and retentions. Trends Parasitol. 24:468–78 [Google Scholar]
  69. Shaver JM, Oldenburg DJ, Bendich AJ. 69.  2008. The structure of chloroplast DNA molecules and the effects of light on the amount of chloroplast DNA during development in Medicago truncatula. Plant Physiol. 146:1064–74 [Google Scholar]
  70. Sheiner L, Vaidya AB, McFadden GI. 70.  2013. The metabolic roles of the endosymbiotic organelles of Toxoplasma and Plasmodium spp. Curr. Opin. Microbiol. 16:452–58 [Google Scholar]
  71. Slamovits CH. 71.  2014. Mitochondrial genomes of alveolates. Mitochondrial Genomes MC Gray 1–6 Berlin: Springer [Google Scholar]
  72. Slamovits CH, Saldarriaga JF, Larocque A, Keeling PJ. 72.  2007. The highly reduced and fragmented mitochondrial genome of the early-branching dinoflagellate Oxyrrhis marina shares characteristics with both apicomplexan and dinoflagellate mitochondrial genomes. J. Mol. Biol. 372:256–68 [Google Scholar]
  73. Smith DR, Lee RW. 73.  2014. A plastid without a genome: evidence from the nonphotosynthetic green algal genus Polytomella. Plant Physiol. 164:1812–19 [Google Scholar]
  74. Vaidya AB, Mather MW. 74.  2009. Mitochondrial evolution and functions in malaria parasites. Annu. Rev. Microbiol. 63:249–67 [Google Scholar]
  75. Van Dooren GG, Kennedy AT, McFadden GI. 75.  2012. The use and abuse of heme in apicomplexan parasites. Antiox. Redox Signal. 17:634–56 [Google Scholar]
  76. Van Dooren GG, Stimmler LH, McFadden GI. 76.  2006. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol. Rev. 30:596–630 [Google Scholar]
  77. Verner Z, Basu S, Benz C, Dixit S, Dobáková E. 77.  et al. 2015. Malleable mitochondrion of Trypanosoma brucei. Int. Rev. Cell. Mol. Biol. 315:73–151 [Google Scholar]
  78. Waller RF, Jackson CJ. 78.  2009. Dinoflagellate mitochondrial genomes: stretching the rules of molecular biology. Bioessays 31:237–45 [Google Scholar]
  79. Wang Y, Morse D. 79.  2006. Rampant polyuridylylation of plastid gene transcripts in the dinoflagellate Lingulodinium. Nucleic Acids Res. 34:613–19 [Google Scholar]
  80. Weatherby K, Carter D. 80.  2013. Chromera velia: the missing link in the evolution of parasitism. Adv. Appl. Microbiol. 85:119–44 [Google Scholar]
  81. Williamson DH, Preiser PR, Moore PW, McCready S, Strath M, Wilson RJM. 81.  2002. The plastid DNA of the malaria parasite Plasmodium falciparum is replicated by two mechanisms. Mol. Microbiol. 45:533–42 [Google Scholar]
  82. Zauner S, Greilinger D, Laatsch T, Kowallik KV, Maier UG. 82.  2004. Substitutional editing of transcripts from genes of cyanobacterial origin in the dinoflagellate Ceratium horridum. FEBS Lett. 577:535–38 [Google Scholar]
  83. Zhang ZD, Green BR, Cavalier-Smith T. 83.  1999. Single gene circles in dinoflagellate chloroplast genomes. Nature 400:155–59 [Google Scholar]
  84. Zhang ZD, Green BR, Cavalier-Smith T. 84.  2000. Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J. Mol. Evol. 51:26–40 [Google Scholar]
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