Missing genes, multiple ORFs, and C-to-U type RNA editing in Acrasis kona (Heterolobosea, Excavata) mitochondrial DNA

Genome Biology and Evolution

Volumn 6, Issue 9, 2014, Pages 2240-2257

  Fu, Cheng Jie ^a   Sheikh, Sanea ^a   Miao, Wei ^b   Andersson, Siv G E ^c   Baldauf, Sandra L ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

Codon usage bias; Discoba; Endosymbiotic gene transfer; Horizontal gene transfer; Plant type RNA editing; Split ribosomal protein gene

Indexed keywords

CODON; MITOCHONDRIAL DNA;

CLASSIFICATION; CODON; EUKARYOTE; GENETICS; HORIZONTAL GENE TRANSFER; MITOCHONDRIAL GENOME; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; RNA EDITING;

BASE SEQUENCE; CODON; DNA, MITOCHONDRIAL; EUKARYOTA; GENE TRANSFER, HORIZONTAL; GENOME, MITOCHONDRIAL; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; RNA EDITING;

EID: 84930357336     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu180     Document Type: Article

References (89)

1. Adams KL, Palmer JD. 2003. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol Phylogenet Evol. 29:380-395.
2. Adl SM, et al. 2012. The revised classification of eukaryotes. J Eukaryot Microbiol. 59:429-493.
3. Benson G. 1999. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27:573-580.
4. Bratlie MS, Johansen J, Drabløs F. 2010. Relationship between operon preference and functional properties of persistent genes in bacterial genomes. BMC Genomics 11:71.
5. Brown MW, Kolisko M, Silberman JD, Roger AJ. 2012. Aggregative multicellularity evolved independently in the eukaryotic supergroup Rhizaria. Curr Biol. 22:1123-1127.
6. Brown MW, Silberman JD, Spiegel FW. 2012. A contemporary evaluation of the acrasids (Acrasidae, Heterolobosea, Excavata). Eur J Protistol. 48:103-123.
7. Burger G, Gray MW, Forget L, Lang BF. 2013. Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol Evol. 5:418-438.
8. Carver T, Thomson N, Bleasby A, Berriman M, Parkhill J. 2009. DNAPlotter: circular and linear interactive genome visualization. Bioinformatics 25:119-120.
9. Carver TJ, et al. 2005. ACT: the Artemis Comparison Tool. Bioinformatics 21:3422-3423.
10. Castresana J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 17:540-552.
11. Cavalier-Smith T, Nikolaev S. 2008. The zooflagellates Stephanopogon and Percolomonas are a clade (class Percolatea: Phylum Percolozoa). J Eukaryot Microbiol. 55:501-509.
12. Clarke M, et al. 2013. Genome of Acanthamoeba castellanii highlights extensive lateral gene transfer and early evolution of tyrosine kinase signaling. Genome Biol. 14:R11.
13. Claros MG, Vincens P. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur J Biochem. 241:779-786.
14. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.
15. Darty K, Denise A, Ponty Y. 2009. VARNA: interactive drawing and editing of the RNA secondary structure. Bioinformatics 25:1974-1975.
16. Darzentas N. 2010. Circoletto: visualizing sequence similarity with Circos. Bioinformatics 26:2620-2621.
17. Dayhoff MO, Schwartz RM, Orcutt BC. 1978. A model of evolutionary change in proteins. In: Dayhoff MO, editor. Atlas of protein sequence and structure. Washington (DC): National Biomedical Research Foundation. p. 345-352.
18. Emanuelsson O, Brunak S, Von Heijne G, Nielsen H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc. 2:953-971.
19. Flegontov P, Gray MW, Burger G, Lukeš J. 2011. Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa? Curr Genet. 57:225-232.
20. Fritz-Laylin LK, et al. 2010. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140:631-642.
21. Fritz-Laylin LK, Ginger ML, Walsh C, Dawson SC, Fulton C. 2011. The Naegleria genome: a free-living microbial eukaryote lends unique insights into core eukaryotic cell biology. Res Microbiol. 162:607-618.
22. Fu C, Xiong J, Miao W. 2009. Genome-wide identification and characterization of cytochrome P450 monooxygenase genes in the ciliate Tetrahymena thermophila. BMC Genomics 10:208.
23. Fujii S, Small I. 2011. The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol. 191:37-47.
24. Gladyshev EA, Meselson M, Arkhipova IR. 2008. Massive horizontal gene transfer in bdelloid rotifers. Science 320:1210-1213.
25. Gray MW. 2012. Evolutionary origin of RNA editing. Biochemistry 51:5235-5242.
26. Gray MW, Lang BF, Burger G. 2004. Mitochondria of protists. Annu Rev Genet. 38:477-524.
27. Hahn C, Bachmann L, Chevreux B. 2013. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads - A baiting and iterative mapping approach. Nucleic Acids Res. 41:e129.
28. Hajduk S, Ochsenreiter T. 2010. RNA editing in kinetoplastids. RNA Biol. 7:229-236.
29. Harding T, et al. 2013. Amoeba stages in the deepest branching heteroloboseans, including Pharyngomonas: evolutionary and systematic implications. Protist 164:272-286.
30. Hayes ML, Giang K, Berhane B, Mulligan RM. 2013. Identification of two pentatricopeptide repeat genes required for RNA editing and zinc binding by c-terminal cytidine deaminase-like domains. J Biol Chem. 288:36519-36529.
31. He D, Fiz-Palacios O, Fu CJ, Tsai CC, Baldauf SL. 2014. An alternative root for the eukaryote tree of life. Curr Biol. 24:465-470.
32. Herman EK, et al. 2013. The mitochondrial genome and a 60-kb nuclear DNA segment from Naegleria fowleri, the causative agent of primary amoebic meningoencephalitis. J Eukaryot Microbiol. 60:179-191.
33. Huang X, Madan A. 1999. CAP3: a DNA sequence assembly program. Genome Res. 9:868-877.
34. Ichinose M, Tasaki E, Sugita C, Sugita M. 2012. A PPR-DYW protein is required for splicing of a group II intron of cox1 pre-mRNA in Physcomitrella patens. Plant J. 70:271-278.
35. Iyer LM, Zhang D, Rogozin IB, Aravind L. 2011. Evolution of the deaminase fold and multiple origins of eukaryotic editing and mutagenic nucleic acid deaminases from bacterial toxin systems. Nucleic Acids Res. 39:9473-9497.
36. Jackman JE, Gott JM, Gray MW. 2012. Doing it in reverse: 30-to-50 polymerization by the Thg1 superfamily. RNA 18:886-899.
37. Jobson RW, Qiu YL. 2008. Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biol Direct. 3:43.
38. Kamikawa R, et al. 2014. Gene content evolution in discobid mitochondria deduced from the phylogenetic position and complete mitochondrial genome of Tsukubamonas globosa. Genome Biol Evol. 6:306-315.
39. Karpenahalli MR, Lupas AN, Söding J. 2007. TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinformatics 8:2.
40. Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 30:772-780.
41. Kiethega GN, Turcotte M, Burger G. 2011. Evolutionarily conserved cox1 trans-splicing without cis-motifs. Mol Biol Evol. 28:2425-2428.
42. Knoop V. 2011. When you can't trust the DNA: RNA editing changes transcript sequences. Cell Mol Life Sci. 68:567-586.
43. Knoop V, Rüdinger M. 2010. DYW-type PPR proteins in a heterolobosean protist: plant RNA editing factors involved in an ancient horizontal gene transfer? FEBS Lett. 584:4287-4291.
44. Lang BF, et al. 1997. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493-497.
45. Lang BF, Gray MW, Burger G. 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu Rev Genet. 33:351-397.
46. Lartillot N, Lepage T, Blanquart S. 2009. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25:2286-2288.
47. Lartillot N, Rodrigue N, Stubbs D, Richer J. 2013. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol. 62:611-615.
48. Laurin-Lemay S, Brinkmann H, Philippe H. 2012. Origin of land plants revisited in the light of sequence contamination and missing data. Curr Biol. 22:R593-R594.
49. Lenz H, Knoop V. 2013. PREPACT 2.0: predicting C-to-U and U-to-C RNA editing in organelle genome sequences with multiple references and curated RNA editing annotation. Bioinform Biol Insights. 7:1-19.
50. Lithgow T, Schneider A. 2010. Evolution of macromolecular import pathways in mitochondria, hydrogenosomes and mitosomes. Philos Trans R Soc Lond B Biol Sci. 365:799-817.
51. Lowe TM, Eddy SR. 1997. TRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955-964.
52. Lukeš J, Hashimi H, Zíková A. 2005. Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet. 48:277-299.
53. Lurin C, et al. 2004. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089-2103.
54. Milne I, et al. 2013. Using Tablet for visual exploration of second-generation sequencing data. Brief Bioinform. 14:193-202.
55. Moreira S, Breton S, Burger G. 2012. Unscrambling genetic information at the RNA level. Wiley Interdiscip Rev RNA. 3:213-228.
56. Novembre JA. 2002. Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol. 19:1390-1394.
57. Okuda K, et al. 2009. Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell 21:146-156.
58. Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T. 2007. Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci USA. 104:8178-8183.
59. Olive LS. 1970. The Mycetozoa: a revised classification. Bot Rev. 36:59-89.
60. Page FC, Blanton RL. 1985. The Heterolobosea (Sarcodina, Rhizopoda), a new class uniting the Schizopyrenida and the Acrasidae (Acrasida). Protistologica 21:121-132.
61. Pánek T, Silberman JD, Yubuki N, Leander BS, Cepicka I. 2012. Diversity, evolution and molecular systematics of the Psalteriomonadidae, the main lineage of anaerobic/microaerophilic heteroloboseans (Excavata: Discoba). Protist 163:807-831.
62. Park JS, Simpson AGB. 2011. Characterization of Pharyngomonas kirbyi (= "Macropharyngomonas halophila" nomen nudum), a very deepbranching, obligately halophilic heterolobosean flagellate. Protist 162:691-709.
63. Ronquist F, et al. 2012. Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 61:539-542.
64. Rüdinger M, Fritz-Laylin L, Polsakiewicz M, Knoop V. 2011. Plant-type mitochondrial RNA editing in the protist Naegleria gruberi. RNA 17:2058-2062.
65. Rüdinger M, Polsakiewicz M, Knoop V. 2008. Organellar RNA editing and plant-specific extensions of pentatricopeptide repeat proteins in jungermanniid but not in marchantiid liverworts. Mol Biol Evol. 25:1405-1414.
66. Rüdinger M, Volkmar U, Lenz H, Groth-Malonek M, Knoop V. 2012. Nuclear DYW-type PPR gene families diversify with increasing RNA editing frequencies in liverwort and moss mitochondria. J Mol Evol. 74:37-51.
67. Rutherford K, et al. 2000. Artemis: sequence visualization and annotation. Bioinformatics 16:944-945.
68. Salinas T, Duchêne AM, Maréchal-Drouard L. 2008. Recent advances in tRNA mitochondrial import. Trends Biochem Sci. 33:320-329.
69. Salone V, et al. 2007. A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett. 581:4132-4138.
70. Schallenberg-Rüdinger M, Lenz H, Polsakiewicz M, Gott JM, Knoop V. 2013. A survey of PPR proteins identifies DYW domains like those of land plant RNA editing factors in diverse eukaryotes. RNA Biol. 10:1343-1350.
71. Simpson AGB, Inagaki Y, Roger AJ. 2006. Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes. Mol Biol Evol. 23:615-625.
72. Sloan DB, MacQueen AH, Alverson AJ, Palmer JD, Taylor DR. 2010. Extensive loss of RNA editing sites in rapidly evolving silene mitochondrial genomes: selection vs. Retroprocessing as the driving force. Genetics 185:1369-1380.
73. Small I, Peeters N, Legeai F, Lurin C. 2004. Predotar: a tool for rapidly screening proteomes for N-terminal targeting sequences. Proteomics 4:1581-1590.
74. Söding J. 2005. Protein homology detection by HMM-HMM comparison. Bioinformatics 21:951-960.
75. Spiegel FW. 1982. The ultrastructure of the trophic cells of the protostelid Planoprotostelium aurantium. Protoplasma 113:165-177.
76. Stamatakis A, et al. 2012. RAxML-Light: a tool for computing terabyte phylogenies. Bioinformatics 28:2064-2066.
77. Swart EC, et al. 2012. The Oxytricha trifallax mitochondrial genome. Genome Biol Evol. 4:136-154.
78. Szklarczyk R, Huynen MA. 2010. Mosaic origin of the mitochondrial proteome. Proteomics 10:4012-4024.
79. Timmis JN, Ayliff MA, Huang CY, Martin W. 2004. Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet. 5:123-135.
80. Visvesvara GS, Moura H, Schuster FL. 2007. Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunol Med Microbiol. 50:1-26.
81. Wang HC, Li K, Susko E, Roger AJ. 2008. A class frequency mixture model that adjusts for site-specific amino acid frequencies and improves inference of protein phylogeny. BMC Evol Biol. 8:331.
82. Watkins RF, Gray MW. 2008. Sampling gene diversity across the supergroup Amoebozoa: large EST data sets from Acanthamoeba castellanii, Hartmannella vermiformis, Physarum polycephalum, Hyperamoeba dachnaya and Hyperamoeba sp. Protist 159:269-281.
83. Wright F. 1990. The "effective number of codons" used in a gene. Gene 87:23-29.
84. Yagi Y, et al. 2013. Pentatricopeptide repeat proteins involved in plant organellar RNA editing. RNA Biol. 10:1236-1242.
85. Yang Q, Sze SH. 2008. Large-scale analysis of gene clustering in bacteria. Genome Res. 18:949-956.
86. Yubuki N, Leander BS. 2008. Ultrastructure and molecular phylogeny of Stephanopogon minuta: an enigmatic microeukaryote from marine interstitial environments. Eur J Protistol. 44:241-253.
87. Zehrmann A, Verbitskiy D, Van Der Merwe JA, Brennicke A, Takenaka M. 2009. A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell 21:558-567.
88. Zhang Z, et al. 2012. Codon Deviation Coefficient: a novel measure for estimating codon usage bias and its statistical significance. BMC Bioinformatics 13:43.
89. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.