リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

リケラボ 全国の大学リポジトリにある学位論文・教授論文を一括検索するならリケラボ論文検索大学・研究所にある論文を検索できる

大学・研究所にある論文を検索できる 「Inventory and Evolution of Mitochondrion-localized Family A DNA Polymerases in Euglenozoa」の論文概要。リケラボ論文検索は、全国の大学リポジトリにある学位論文・教授論文を一括検索できる論文検索サービスです。

コピーが完了しました

URLをコピーしました

論文の公開元へ論文の公開元へ
書き出し

Inventory and Evolution of Mitochondrion-localized Family A DNA Polymerases in Euglenozoa

平川, 泰久 稲垣, 祐司 HARADA, Ryo YABUKI, Akinori KASHIYAMA, Yuichiro MARUYAMA, Moe ONUMA, Ryo SOUKAL, Petr MIYAGISHIMA, Shinya HAMPL, Vladimír TANIFUJI, Goro 筑波大学 DOI:10.3390/pathogens9040257

2020.04.09

概要

The order Trypanosomatida has been well studied due to its pathogenicity and the unique biology of the mitochondrion. In Trypanosoma brucei, four DNA polymerases, namely PolIA, PolIB, PolIC, and PolID, related to bacterial DNA polymerase I (PolI), were shown to be localized in mitochondria experimentally. These mitochondrion-localized DNA polymerases are phylogenetically distinct from other family A DNA polymerases, such as bacterial PolI, DNA polymerase gamma (Polγ) in human and yeasts, “plant and protist organellar DNA polymerase (POP)” in diverse eukaryotes. However, the diversity of mitochondrion-localized DNA polymerases in Euglenozoa other than Trypanosomatida is poorly understood. In this study, we discovered putative mitochondrion-localized DNA polymerases in broad members of three major classes of Euglenozoa—Kinetoplastea, Diplonemea, and Euglenida—to explore the origin and evolution of trypanosomatid PolIA-D. We unveiled distinct inventories of mitochondrion-localized DNA polymerases in the three classes: (1) PolIA is ubiquitous across the three euglenozoan classes, (2) PolIB, C, and D are restricted in kinetoplastids, (3) new types of mitochondrion-localized DNA polymerases were identified in a prokinetoplastid and diplonemids, and (4) evolutionarily distinct types of POP were found in euglenids. We finally propose scenarios to explain the inventories of mitochondrion-localized DNA polymerases in Kinetoplastea, Diplonemea, and Euglenida.

参考文献

1. Barrett, M.P.; Burchmore, R.J.S.; Stich, A.; Lazzari, J.O.; Frasch, A.C.; Cazzulo, J.J.; Krishna, S. The trypanosomiases. Lancet 2003, 362, 1469–1480. [CrossRef]

2. Verner, Z.; Basu, S.; Benz, C.; Dixit, S.; Dobáková, E.; Faktorová, D.; Hashimi, H.; Horáková, E.; Huang, Z.; Paris, Z.; et al. Malleable mitochondrion of Trypanosoma brucei. In International Review of Cell and Molecular Biology; Academic Press: Cambridge, MA, USA, 2015; Volume 315, pp. 73–151.

3. Klingbeil, M.M.; Motyka, S.A.; Englund, P.T. Multiple mitochondrial DNA polymerases in Trypanosoma brucei. Mol. Cell 2002, 10, 175–186. [CrossRef]

4. Krasich, R.; Copeland, W.C. DNA polymerases in the mitochondria: A critical review of the evidence. Physiol. Behav. 2017, 22, 692–709.

5. Saxowsky, T.T.; Choudhary, G.; Klingbeil, M.M.; Englund, P.T. Trypanosoma brucei has two distinct mitochondrial DNA polymerase β enzymes. J. Biol. Chem. 2003, 278, 49095–49101. [CrossRef]

6. Rajão, M.A.; Passos-Silva, D.G.; DaRocha, W.D.; Franco, G.R.; Macedo, A.M.; Pena, S.D.J.; Teixeira, S.M.; Machado, C.R. DNA polymerase kappa from Trypanosoma cruzi localizes to the mitochondria, bypasses 8-oxoguanine lesions and performs DNA synthesis in a recombination intermediate. Mol. Microbiol. 2009, 71, 185–197. [CrossRef] [PubMed]

7. Graziewicz, M.A.; Longley, M.J.; Copeland, W.C. DNA polymerase γ in mitochondrial DNA replication and repair. Chem. Rev. 2006, 106, 383–405. [CrossRef] [PubMed]

8. Christensen, A.C.; Lyznik, A.; Mohammed, S.; Elowsky, C.G.; Elo, A.; Yule, R.; Mackenzie, S.A. Dual-domain, dual-targeting organellar protein presequences in Arabidopsis can use non-AUG start codons. Plant Cell 2005, 17, 2805–2816. [CrossRef] [PubMed]

9. Moriyama, T.; Sato, N. Enzymes involved in organellar DNA replication in photosynthetic eukaryotes. Front. Plant Sci. 2014, 5, 480:1–480:12. [CrossRef]

10. Hirakawa, Y.; Watanabe, A. Organellar DNA polymerases in complex plastid-bearing algae. Biomolecules 2019, 9, 140. [CrossRef]

11. Adl, S.M.; Bass, D.; Lane, C.E.; Lukeš, J.; Schoch, C.L.; Smirnov, A.; Agatha, S.; Berney, C.; Brown, M.W.; Burki, F.; et al. Revisions to the classification, nomenclature, and diversity of eukaryotes. J. Eukaryot. Microbiol. 2019, 66, 4–119. [CrossRef]

12. Lukeš, J.; Guilbride, D.L.; Votýpka, J.; Zíková, A.; Benne, R.; Englund, P.T. Kinetoplast DNA network: Evolution of an improbable structure. Eukayot. Cell 2002, 1, 495–502. [CrossRef] [PubMed]

13. David, V.; Flegontov, P.; Gerasimov, E.; Tanifuji, G.; Hashimi, H.; Logacheva, M.D.; Maruyama, S.; Onodera, N.T.; Gray, M.W.; Archibald, J.M.; et al. Gene loss and error-prone RNA editing in the mitochondrion of Perkinsela, an endosymbiotic kinetoplastid. MBio 2015, 6, e01498-15:1–e01498-15:12. [CrossRef] [PubMed]

14. Yabuki, A.; Tanifuji, G.; Kusaka, C.; Takishita, K.; Fujikura, K. Hyper-eccentric structural genes in the mitochondrial genome of the algal parasite Hemistasia phaeocysticola. Genome Biol. Evol. 2016, 8, 2870–2878. [PubMed]

15. Burger, G.; Valach, M. Perfection of eccentricity: Mitochondrial genomes of diplonemids. IUBMB Life 2018, 70, 1197–1206. [CrossRef]

16. Kaur, B.; Záhonová, K.; Valach, M.; Faktorová, D.; Prokopchuk, G.; Burger, G.; Lukeš, J. Gene fragmentation and RNA editing without borders: Eccentric mitochondrial genomes of diplonemids. Nucleic Acids Res. 2020, 48, 2694–2708. [CrossRef]

17. Roy, J.; Faktorová, D.; Lukeš, J.; Burger, G. Unusual mitochondrial genome structures throughout the Euglenozoa. Protist 2007, 158, 385–396. [CrossRef]

18. Spencer, D.F.; Gray, M.W. Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: Fragmented genes in a seemingly fragmented genome. Mol. Genet. Genom. 2011, 285, 19–31. [CrossRef]

19. Dobáková, E.; Flegontov, P.; Skalický, T.; Lukeš, J. Unexpectedly streamlined mitochondrial genome of the euglenozoan Euglena gracilis. Genome Biol. Evol. 2015, 7, 3358–3367. [CrossRef]

20. Simpson, A.G.B.; Hoff, J.V.D.; Bernard, C.; Burton, H.R.; Patterson, D.J. The ultrastructure and systematic position of the euglenozoon Postgaardi mariagerensis. Arch. Protistenkd. 1997, 147, 213–225. [CrossRef]

21. Yubuki, N.; Edgcomb, V.P.; Bernhard, J.M.; Leander, B.S. Ultrastructure and molecular phylogeny of Calkinsia aureus: Cellular identity of a novel clade of deep-sea euglenozoans with epibiotic bacteria. BMC Microbiol. 2009, 9, 16:1–16:22. [CrossRef]

22. Breglia, S.A.; Yubuki, N.; Hoppenrath, M.; Leander, B.S. Ultrastructure and molecular phylogenetic position of a novel euglenozoan with extrusive episymbiotic bacteria: Bihospites bacati n. gen. et sp. (Symbiontida). BMC Microbiol. 2010, 10, 145:1–145:21. [CrossRef]

23. Moriyama, T.; Terasawa, K.; Fujiwara, M.; Sato, N. Purification and characterization of organellar DNA polymerases in the red alga Cyanidioschyzon merolae. FEBS J. 2008, 275, 2899–2918. [CrossRef] [PubMed]

24. Chandler, J.; Vandoros, A.V.; Mozeleski, B.; Klingbeil, M.M. Stem-loop silencing reveals that a third mitochondrial DNA polymerase, POLID, is required for kinetoplast DNA replication in trypanosomes. Eukaryot. Cell 2008, 7, 2141–2146. [CrossRef] [PubMed]

25. Bruhn, D.F.; Mozeleski, B.; Falkin, L.; Klingbeil, M.M. Mitochondrial DNA polymerase POLIB is essential for minicircle DNA replication in African trypanosomes. Mol. Microbiol. 2010, 75, 1414–1425. [CrossRef] [PubMed]

26. Bruhn, D.F.; Sammartino, M.P.; Klingbeil, M.M. Three mitochondrial DNA polymerases are essential for kinetoplast DNA replication and survival of bloodstream form Trypanosoma brucei. Eukaryot. Cell 2011, 10, 734–743. [CrossRef] [PubMed]

27. Panigrahi, A.K.; Ogata, Y.; Zíková, A.; Anupama, A.; Dalley, R.A.; Acestor, N.; Myler, P.J.; Stuart, K.D. A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 2009, 9, 434–450. [CrossRef]

28. Hammond, M.J.; Nenarokova, A.; Butenko, A.; Zoltner, M.; Dobáková, E.L.; Field, M.C.; Lukeš, J. A uniquely complex mitochondrial proteome from Euglena gracilis. Mol. Biol. Evol. 2020. Epub ahead of print. [CrossRef]

29. Emanuelsson, O.; Nielsen, H.; Brunak, S.; Heijne, G.V. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300, 1005–1016. [CrossRef]

30. Kume, K.; Amagasa, T.; Hashimoto, T.; Kitagawa, H. NommPred: Prediction of mitochondrial and mitochondrion-related organelle proteins of nonmodel organisms. Evol. Bioinform. 2018, 14, 1–12. [CrossRef]

31. Petsalaki, E.I.; Bagos, P.G.; Litou, Z.I.; Hamodrakas, S.J. PredSL: A tool for the N-terminal sequence-based prediction of protein subcellular localization. Genom. Proteom. Bioinf. 2006, 4, 48–55. [CrossRef]

32. Fukasawa, Y.; Tsuji, J.; Fu, S.C.; Tomii, K.; Horton, P.; Imai, K. MitoFates: Improved prediction of mitochondrial targeting sequences and their cleavage sites. Mol. Cell. Proteomics 2015, 14, 1113–1126. [CrossRef] [PubMed]

33. Bicudo, C.E.d.M.; Menezes, M. Phylogeny and classification of Euglenophyceae: A brief review. Front. Ecol. Evol. 2016, 4, 17:1–17:15. [CrossRef]

34. Tashyreva, D.; Prokopchuk, G.; Yabuki, A.; Kaur, B.; Faktorová, D.; Votýpka, J.; Kusaka, C.; Fujikura, K.; Shiratori, T.; Ishida, K.I.; et al. Phylogeny and morphology of new diplonemids from Japan. Protist 2018, 169, 158–179. [CrossRef] [PubMed]

35. Yazaki, E.; Ishikawa, S.A.; Kume, K.; Kumagai, A.; Kamaishi, T.; Tanifuji, G.; Hashimoto, T.; Inagaki, Y. Global kinetoplastea phylogeny inferred from a large-scale multigene alignment including parasitic species for better understanding transitions from a free-living to a parasitic lifestyle. Genes Genet. Syst. 2017, 92, 35–42. [CrossRef] [PubMed]

36. Tosal, L.; Comendador, M.A.; Sierra, L.M. The mus308 locus of Drosophila melanogaster is implicated in the bypass of ENU-induced O-alkylpyrimidine adducts. Mol. Gen. Genet. 2000, 263, 144–151. [CrossRef] [PubMed]

37. Concepción-Acevedo, J.; Miller, J.C.; Boucher, M.J.; Klingbeil, M.M. Cell cycle localization dynamics of mitochondrial DNA polymerase IC in African trypanosomes. Mol. Biol. Cell 2018, 29, 2540–2552. [CrossRef] [PubMed]

38. Ono, Y.; Sakai, A.; Takechi, K.; Takio, S.; Takusagawa, M.; Takano, H. NtPolI-like1 and NtPolI-like2, bacterial DNA polymerase I homologs isolated from BY-2 cultured tobacco cells, encode DNA polymerases engaged in DNA replication in both plastids and mitochondria. Plant Cell Physiol. 2007, 48, 1679–1692. [CrossRef]

39. Moriyama, T.; Tajima, N.; Sekine, K.; Sato, N. Localization and phylogenetic analysis of enzymes related to organellar genome replication in the unicellular rhodophyte Cyanidioschyzon merolae. Genome Biol. Evol. 2014, 6, 228–237. [CrossRef]

40. Bendtsen, J.D.; Nielsen, H.; Heijne, G.V.; Brunak, S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340, 783–795. [CrossRef]

41. Krogh, A.; Larsson, B.; Heijne, G.V.; Sonnhammer, E.L.L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 2001, 305, 567–580. [CrossRef]

42. Novák Vanclová, A.M.G.; Zoltner, M.; Kelly, S.; Soukal, P.; Záhonová, K.; Füssy, Z.; Ebenezer, T.E.; Lacová Dobáková, E.; Eliáš, M.; Lukeš, J.; et al. Metabolic quirks and the colourful history of the Euglena gracilis secondary plastid. New Phytol. 2020, 225, 1578–1592. [CrossRef] [PubMed]

43. Tanifuji, G.; Cenci, U.; Moog, D.; Dean, S.; Nakayama, T.; David, V.; Fiala, I.; Curtis, B.A.; Sibbald, S.J.; Onodera, N.T.; et al. Genome sequencing reveals metabolic and cellular interdependence in an amoeba-kinetoplastid symbiosis. Sci. Rep. 2017, 7, 11688:1–11688:13. [CrossRef] [PubMed]

44. Turmel, M.; Gagnon, M.C.; O’Kelly, C.J.; Otis, C.; Lemieux, C. The chloroplast genomes of the green algae Pyramimonas, Monomastix, and Pycnococcus shed new light on the evolutionary history of prasinophytes and the origin of the secondary chloroplasts of euglenids. Mol. Biol. Evol. 2009, 26, 631–648. [CrossRef] [PubMed]

45. Suzuki, S.; Hirakawa, Y.; Kofuji, R.; Sugita, M.; Ishida, K. Plastid genome sequences of Gymnochlora stellata, Lotharella vacuolata, and Partenskyella glossopodia reveal remarkable structural conservation among chlorarachniophyte species. J. Plant Res. 2016, 129, 581–590. [CrossRef]

46. Sayers, E.W.; Beck, J.; Brister, J.R.; Bolton, E.E.; Canese, K.; Comeau, D.C.; Funk, K.; Ketter, A.; Kim, S.; Kimchi, A.; et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2020, 48, D9–D16. [CrossRef]

47. Chen, S.; Zhou, Y.; Chen, Y.; Gu, J. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018, 34, i884–i890. [CrossRef]

48. Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.; et al. Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nat. Biotechnol. 2011, 29, 644–652. [CrossRef]

49. Camacho, C.; Coulouris, G.; Avagyan, V.; Ma, N.; Papadopoulos, J.; Bealer, K.; Madden, T.L. BLAST+: Architecture and applications. BMC Bioinform. 2009, 10, 421:1–421:9. [CrossRef]

50. Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013, 30, 772–780. [CrossRef]

51. Capella-Gutiérrez, S.; Silla-Martínez, J.M.; Gabaldón, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25, 1972–1973. [CrossRef]

52. Nguyen, L.T.; Schmidt, H.A.; Von Haeseler, A.; Minh, B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015, 32, 268–274. [CrossRef] [PubMed]

53. Kalyaanamoorthy, S.; Minh, B.Q.; Wong, T.K.F.; Von Haeseler, A.; Jermiin, L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 2017, 14, 587–589. [CrossRef] [PubMed]

54. Lartillot, N.; Lepage, T.; Blanquart, S. PhyloBayes 3: Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 2009, 25, 2286–2288. [CrossRef] [PubMed]

55. Eddy, S.R. HMMER: Biosequence Analysis Using Profile Hidden Markov Models. Available online: http://hmmer.org/ (accessed on 10 December 2019).

56. El-Gebali, S.; Mistry, J.; Bateman, A.; Eddy, S.R.; Luciani, A.; Potter, S.C.; Qureshi, M.; Richardson, L.J.; Salazar, G.A.; Smart, A.; et al. The Pfam protein families database in 2019. Nucleic Acids Res. 2019, 47, D427–D432. [CrossRef]

57. López-García, P.; Duperron, S.; Philippot, P.; Foriel, J.; Susini, J.; Moreira, D. Bacterial diversity in hydrothermal sediment and epsilonproteobacterial dominance in experimental microcolonizers at the Mid-Atlantic Ridge. Environ. Microbiol. 2003, 5, 961–976. [CrossRef]

58. Scheckenbach, F.; Hausmann, K.; Wylezich, C.; Weitere, M.; Arndt, H. Large-scale patterns in biodiversity of microbial eukaryotes from the abyssal sea floor. Proc. Natl. Acad. Sci. USA 2010, 107, 115–120. [CrossRef]

59. Marquardt, M.; Vader, A.; Stübner, E.I.; Reigstad, M.; Gabrielsen, T.M. Strong seasonality of marine microbial eukaryotes in a high-Arctic fjord (Isfjorden, in West Spitsbergen, Norway). Appl. Environ. Microbiol. 2016, 82, 1868–1880. [CrossRef]

60. Gawryluk, R.M.R.; del Campo, J.; Okamoto, N.; Strassert, J.F.H.; Lukeš, J.; Richards, T.A.; Worden, A.Z.; Santoro, A.E.; Keeling, P.J. Morphological identification and single-cell genomics of marine diplonemids. Curr. Biol. 2016, 26, 3053–3059. [CrossRef]

61. Wideman, J.G.; Lax, G.; Leonard, G.; Milner, D.S.; Rodríguez-Martínez, R.; Simpson, A.G.B.; Richards, T.A. A single-cell genome reveals diplonemid-like ancestry of kinetoplastid mitochondrial gene structure. Philos. Trans. R. Soc. B Biol. Sci. 2019, 374, 20190100. [CrossRef]

参考文献をもっと見る