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Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes


Two scenarios have been proposed to describe the history of cellular life on our planet. For some authors, two lineages emerged from the last universal cellular ancestor, one leading to Bacteria, the other one leading to a common ancestor of Archaea and Eukarya (Woese’s hypothesis), while others suggest that Eukaryotes emerged from within an archaeal subgroup (eocyte hypothesis). This latter hypothesis has been boosted by the reconstruction of new archaeal genomes from environmental DNA. These analyses have suggested that eukaryotes originated from complex archaea, called Lokiarchaeota, the first described members of the recently proposed Asgard superphylum. Considering the importance of this question, we performed new analyses of the universal proteins from Lokiarchaea and realized that their affiliation to Eukaryotes was most probably due to different biases, including chimeric sequences and unequal rate of protein evolution. From our results, we suggest here that Lokiarchaea and close relatives are sister group to Euryarchaeota, not to Eukarya. Notably, we also show that the choices of the universal markers to include in one’s analysis will critically impact the scenario supported and that some markers as the RNA polymerase support the traditional Woese’s tree.


Vyšlo v časopise: Lokiarchaea are close relatives of Euryarchaeota, not bridging the gap between prokaryotes and eukaryotes. PLoS Genet 13(6): e32767. doi:10.1371/journal.pgen.1006810
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1006810

Souhrn

Two scenarios have been proposed to describe the history of cellular life on our planet. For some authors, two lineages emerged from the last universal cellular ancestor, one leading to Bacteria, the other one leading to a common ancestor of Archaea and Eukarya (Woese’s hypothesis), while others suggest that Eukaryotes emerged from within an archaeal subgroup (eocyte hypothesis). This latter hypothesis has been boosted by the reconstruction of new archaeal genomes from environmental DNA. These analyses have suggested that eukaryotes originated from complex archaea, called Lokiarchaeota, the first described members of the recently proposed Asgard superphylum. Considering the importance of this question, we performed new analyses of the universal proteins from Lokiarchaea and realized that their affiliation to Eukaryotes was most probably due to different biases, including chimeric sequences and unequal rate of protein evolution. From our results, we suggest here that Lokiarchaea and close relatives are sister group to Euryarchaeota, not to Eukarya. Notably, we also show that the choices of the universal markers to include in one’s analysis will critically impact the scenario supported and that some markers as the RNA polymerase support the traditional Woese’s tree.


Zdroje

1. Embley TM, Martin W. Eukaryotic evolution, changes and challenges. Nature. 2006;440: 623–630. doi: 10.1038/nature04546 16572163

2. Criscuolo A, Gribaldo S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol Biol. 2010;10: 210. doi: 10.1186/1471-2148-10-210 20626897

3. Martijn J, Ettema TJG. From archaeon to eukaryote: the evolutionary dark ages of the eukaryotic cell. Biochem Soc Trans. 2013;41: 451–7. doi: 10.1042/BST20120292 23356327

4. Forterre P. The common ancestor of archaea and eukarya was not an archaeon. Archaea. 2013;2013. doi: 10.1155/2013/372396 24348094

5. Forterre P. The universal tree of life: An update. Front Microbiol. 2015;6: 1–18. doi: 10.3389/fmicb.2015.00717

6. López-García P, Moreira D. Open Questions on the Origin of Eukaryotes. Trends Ecol Evol. 2015;30: 697–708. doi: 10.1016/j.tree.2015.09.005 26455774

7. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87: 4576–4579. doi: 10.1073/pnas.87.12.4576 2112744

8. Lake JA, Henderson E, Oakes M, Clark MW. Eocytes: a new ribosome structure indicates a kingdom with a close relationship to eukaryotes. Proc Natl Acad Sci U S A. 1984;81: 3786–3790. doi: 10.1073/pnas.81.12.3786 6587394

9. Gouy R, Baurain D, Philippe H. Rooting the tree of life: the phylogenetic jury is still out. Philos Trans R Soc Lond B Biol Sci. 2015;370: 20140329. doi: 10.1098/rstb.2014.0329 26323760

10. Penny D, Collins LJ, Daly TK, Cox SJ. The Relative Ages of Eukaryotes and Akaryotes. J Mol Evol. 2014;79: 228–239. doi: 10.1007/s00239-014-9643-y 25179144

11. Koonin E V. Archaeal ancestors of eukaryotes: not so elusive any more. BMC Biol. BMC Biology; 2015;13: 84. doi: 10.1186/s12915-015-0194-5 26437773

12. Lane N, Martin W. The energetics of genome complexity. Nature. Nature Publishing Group; 2010;467: 929–34. doi: 10.1038/nature09486 20962839

13. Embley TM, Williams TA. Steps on the road to eukaryotes. Nature. 2015;521: 169–170. doi: 10.1038/nature14522 25945740

14. Spang A, Saw JH, Jørgensen SL, Zaremba-Niedzwiedzka K, Martijn J, Lind AE, et al. Complex archaea that bridge the gap between prokaryotes and eukaryotes. Nature. 2015;521: 173–179. doi: 10.1038/nature14447 25945739

15. Jorgensen SL, Thorseth IH, Pedersen RB, Baumberger T, Schleper C. Quantitative and phylogenetic study of the deep sea archaeal group in sediments of the arctic mid-ocean spreading ridge. Front Microbiol. 2013;4: 1–11. doi: 10.3389/fmicb.2013.00299

16. Takai K, Komatsu T, Inagaki F, Horikoshi K. Distribution of Archaea in a Black Smoker Chimney Structure. Appl Environ Microbiol. 2001;67: 3618–3629. doi: 10.1128/AEM.67.8.3618-3629.2001 11472939

17. Knittel K, Lösekann T, Boetius A, Kort R, Amann R, Lo T. Diversity and Distribution of Methanotrophic Archaea at Cold Seeps Diversity and Distribution of Methanotrophic Archaea at Cold Seeps †. Appl Environ Microbiol. 2005;71: 467–479. doi: 10.1128/AEM.71.1.467-479.2005 15640223

18. Guy L, Ettema TJG. The archaeal “TACK” superphylum and the origin of eukaryotes. Trends Microbiol. Elsevier Ltd; 2011;19: 580–587. doi: 10.1016/j.tim.2011.09.002 22018741

19. Koonin E V. Origin of eukaryotes from within archaea, archaeal eukaryome and bursts of gene gain: eukaryogenesis just made easier? Philos Trans R Soc Lond B Biol Sci. 2015;370: 20140333. doi: 10.1098/rstb.2014.0333 26323764

20. Villanueva L, Schouten S, Sinninghe Damsté JS. Phylogenomic analysis of lipid biosynthetic genes of Archaea shed light on the “lipid divide.” Environ Microbiol. 2016;0. doi: 10.1002/000.13361

21. Surkont J, Pereira-Leal JB. Are there Rab GTPases in Archaea? Mol Biol Evol. 2016;33: 1–24. doi: 10.1093/molbev/msw061

22. Klinger CM, Spang A, Dacks JB, Ettema TJG. Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol Biol Evol. 2016;33: msw034-. doi: 10.1093/molbev/msw034 26893300

23. Sousa FL, Neukirchen S, Allen JF, Lane N, Martin WF. Lokiarchaeon is hydrogen dependent. Nat Microbiol. Nature Publishing Group; 2016;1: 16034. doi: 10.1038/nmicrobiol.2016.34 27572645

24. Mariotti M, Lobanov A V., Manta B, Santesmasses D, Bofill A, Guigó R, et al. Lokiarchaeota Marks the Transition between the Archaeal and Eukaryotic Selenocysteine Encoding Systems. Mol Biol Evol. 2016;33: 2441–2453. doi: 10.1093/molbev/msw122 27413050

25. Nasir A, Kim KM, Caetano-Anollés G. Lokiarchaeota: Eukaryote-like missing links from microbial dark matter? Trends Microbiol. 2015;23: 448–450. doi: 10.1016/j.tim.2015.06.001 26112912

26. Nasir A, Kim KM, Da Cunha V, Caetano-Anollés G, S G. Arguments Reinforcing the Three-Domain View of Diversified Cellular Life. Archaea. 2016;2016: 1–11. doi: 10.1155/2016/1851865 28050162

27. Brochier C, Forterre P, Gribaldo S. An emerging phylogenetic core of Archaea: phylogenies of transcription and translation machineries converge following addition of new genome sequences. BMC Evol Biol. 2005;5: 36. doi: 10.1186/1471-2148-5-36 15932645

28. Brinkmann H, van der Giezen M, Zhou Y, Poncelin de Raucourt G, Philippe H. An empirical assessment of long-branch attraction artefacts in deep eukaryotic phylogenomics. Syst Biol. 2005;54: 743–757. doi: 10.1080/10635150500234609 16243762

29. Bodilis J, Nsigue Meilo S, Cornelis P, De Vos P, Barray S. A long-branch attraction artifact reveals an adaptive radiation in pseudomonas. Mol Biol Evol. 2011;28: 2723–2726. doi: 10.1093/molbev/msr099 21504889

30. Seitz KW, Lazar CS, Hinrichs K-U, Teske AP, Baker BJ. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J. Nature Publishing Group; 2016; 1–10. doi: 10.1038/ismej.2015.233 26824177

31. Zaremba-Niedzwiedzka K, Caceres E, Saw J, Backstrom D, Juzokaite L, Vancaester E, et al. Metagenomic exploration of Asgard arcahea illuminates the origin of eukaryotic cellular complexity. Nature. 2017;541: 353–358. doi: 10.1038/nature21031 28077874

32. Brochier C, Forterre P, Gribaldo S. Archaeal phylogeny based on proteins of the transcription and translation machineries: tackling the Methanopyrus kandleri paradox. Genome Biol. 2004;5: R17. doi: 10.1186/gb-2004-5-3-r17 15003120

33. Brochier C, Gribaldo S, Zivanovic Y, Confalonieri F, Forterre P. Nanoarchaea: representatives of a novel archaeal phylum or a fast-evolving euryarchaeal lineage related to Thermococcales? Genome Biol. 2005;6: R42. doi: 10.1186/gb-2005-6-5-r42 15892870

34. Petitjean C, Deschamps P, López-Garciá P, Moreira D. Rooting the domain archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol Evol. 2014;7: 191–204. doi: 10.1093/gbe/evu274 25527841

35. Elkins JG, Podar M, Graham DE, Makarova KS, Wolf Y, Randau L, et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc Natl Acad Sci U S A. 2008;105: 8102–8107. doi: 10.1073/pnas.0801980105 18535141

36. Rinke C, Schwientek P, Sczyrba A, Ivanova NN, Anderson IJ, Cheng J-F, et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature. Nature Publishing Group; 2013;499: 431–437. doi: 10.1038/nature12352 23851394

37. Lartillot N, Brinkmann H, Philippe H. Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol. 2007;7 Suppl 1: S4. doi: 10.1186/1471-2148-7-S1-S4 17288577

38. Brochier-Armanet C, Forterre P, Gribaldo S. Phylogeny and evolution of the Archaea: One hundred genomes later. Curr Opin Microbiol. 2011;14: 274–281. doi: 10.1016/j.mib.2011.04.015 21632276

39. Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P. Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol. 2008;6: 245–252. doi: 10.1038/nrmicro1852 18274537

40. Shimodaira H. An Approximately Unbiased Test of Phylogenetic Tree Selection. Syst Biol. 2002;51: 492–508. doi: 10.1080/10635150290069913 12079646

41. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25: 1043–55. doi: 10.1101/gr.186072.114 25977477

42. Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, et al. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3: e1319. doi: 10.7717/peerj.1319 26500826

43. Le Calvez T, Burgaud G, Mah?? S, Barbier G, Vandenkoornhuyse P. Fungal diversity in deep-sea hydrothermal ecosystems. Appl Environ Microbiol. 2009;75: 6415–6421. doi: 10.1128/AEM.00653-09 19633124

44. Mahé S, Rédou V, Le Calvez T, Vandenkoornhuyse P, Burgaud G. Fungi in deep-sea environments and metagenomics. The Ecological Genomics of Fungi. 2014. doi: 10.1002/9781118735893.ch15

45. Ivarsson M, Schnürer A, Bengtson S, Neubeck A. Anaerobic Fungi: A Potential Source of Biological H 2 in the Oceanic Crust. Front Microbiol. 2016;7: 1–8. doi: 10.3389/fmicb.2016.00674

46. Amend A. From Dandruff to Deep-Sea Vents: Malassezia-like Fungi Are Ecologically Hyper-diverse. PLoS Pathog. 2014;10: 8–11. doi: 10.1371/journal.ppat.1004277 25144294

47. Nagahama T, Nagano Y. Cultured and uncultured fungal diversity in deep-sea environments. Prog Mol Subcell Biol. United States; 2012;53: 173–187. doi: 10.1007/978-3-642-23342-5_9 22222832

48. Orsi W, Biddle JF, Edgcomb V. Deep Sequencing of Subseafloor Eukaryotic rRNA Reveals Active Fungi across Marine Subsurface Provinces. PLoS One. 2013;8. doi: 10.1371/journal.pone.0056335 23418556

49. Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, et al. Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol. 2013;20: 714–737. doi: 10.1089/cmb.2013.0084 24093227

50. Lasken RS, Stockwell TB. Mechanism of chimera formation during the Multiple Displacement Amplification reaction. BMC Biotechnol. 2007;7: 19. doi: 10.1186/1472-6750-7-19 17430586

51. Bankevich A, Nurk S, Antipov D, Gurevich A a., Dvorkin M, Kulikov AS, et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J Comput Biol. 2012;19: 455–477. doi: 10.1089/cmb.2012.0021 22506599

52. Castelle CJ, Wrighton KC, Thomas BC, Hug LA, Brown CT, Wilkins MJ, et al. Genomic expansion of domain archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr Biol. Elsevier Ltd; 2015;25: 690–701. doi: 10.1016/j.cub.2015.01.014 25702576

53. Meng J, Xu J, Qin D, He Y, Xiao X, Wang F. Genetic and functional properties of uncultivated MCG archaea assessed by metagenome and gene expression analyses. ISME J. Nature Publishing Group; 2013;8: 650–659. doi: 10.1038/ismej.2013.174 24108328

54. Baker BJ, Saw JH, Lind AE, Lazar CS, Hinrichs K, Teske AP, et al. Genomic inference of the metabolism of cosmopolitan subsurface Archaea, Hadesarchaea. Nat Microbiol. Nature Publishing Group; 2016;1: 16002. doi: 10.1038/nmicrobiol.2016.2 27572167

55. Mwirichia R, Alam I, Rashid M, Vinu M, Ba-Alawi W, Anthony Kamau A, et al. Metabolic traits of an uncultured archaeal lineage -MSBL1- from brine pools of the Red Sea. Sci Rep. 2016;6: 19181. doi: 10.1038/srep19181 26758088

56. Atkinson GC. The evolutionary and functional diversity of classical and lesser-known cytoplasmic and organellar translational GTPases across the tree of life. BMC Genomics. 2015;16: 78. doi: 10.1186/s12864-015-1289-7 25756599

57. Shen X, Hittinger CT, Rokas A. Studies Can Be Driven By a Handful of Genes. Nat Ecol Evol. Macmillan Publishers Limited, part of Springer Nature.; 2017;1: 126. doi: 10.1038/s41559-017-0126

58. Williams TA, Foster PG, Nye TMW, Cox CJ, Embley TM. A congruent phylogenomic signal places eukaryotes within the Archaea. Proc Biol Sci. 2012;279: 4870–9. doi: 10.1098/rspb.2012.1795 23097517

59. Cox CJ, Foster PG, Hirt RP, Harris SR, Embley TM. The archaebacterial origin of eukaryotes. Proc Natl Acad Sci U S A. 2008;105: 20356–61. doi: 10.1073/pnas.0810647105 19073919

60. Williams TA, Embley TM. Archaeal “dark matter” and the origin of eukaryotes. Genome Biol Evol. 2014;6: 474–481. doi: 10.1093/gbe/evu031 24532674

61. Lasek-Nesselquist E, Gogarten JP. The effects of model choice and mitigating bias on the ribosomal tree of life. Mol Phylogenet Evol. Elsevier Inc.; 2013;69: 17–38. doi: 10.1016/j.ympev.2013.05.006 23707703

62. Leigh JW, Lapointe F-J, Lopez P, Bapteste E. Evaluating Phylogenetic Congruence in the Post-Genomic. Genome Biol Evol. 2011;3: 571–587. doi: 10.1093/gbe/evr050 21712432

63. Wolf YI, Koonin E V. Genome reduction as the dominant mode of evolution. Bioessays. 2013;35: 829–837. doi: 10.1002/bies.201300037 23801028

64. Yutin N, Puigbo P, Koonin E V, Wolf YI. Phylogenomics of Prokaryotic Ribosomal Proteins. PLoS One. 2012;7. doi: 10.1371/Citation

65. Visweswaran GRR, Dijkstra BW, Kok J. Murein and pseudomurein cell wall binding domains of bacteria and archaea—a comparative view. Appl Microbiol Biotechnol. 2011;92: 921–928. doi: 10.1007/s00253-011-3637-0 22012341

66. Steenbakkers PJM, Geerts WJ, Ayman-Oz NA, Keltjens JT. Identification of pseudomurein cell wall binding domains. Mol Microbiol. 2006;62: 1618–1630. doi: 10.1111/j.1365-2958.2006.05483.x 17427286

67. Katz LA, Grant JR. Taxon-rich phylogenomic analyses resolve the eukaryotic tree of life and reveal the power of subsampling by sites. Syst Biol. 2015;64: 406–415. doi: 10.1093/sysbio/syu126 25540455

68. Raymann K, Brochier-Armanet C, Gribaldo S. The two-domain tree of life is linked to a new root for the Archaea. Proc Natl Acad Sci U S A. 2015;112: 6670–5. doi: 10.1073/pnas.1420858112 25964353

69. Gouy M, Guindon S, Gascuel O. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27: 221–4. doi: 10.1093/molbev/msp259 19854763

70. Löytynoja A, Goldman N. An algorithm for progressive multiple alignment of sequences with insertions. Proc Natl Acad Sci U S A. 2005;102: 10557–62. doi: 10.1073/pnas.0409137102 16000407

71. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol Biol Evol. 2013;30: 772–780. doi: 10.1093/molbev/mst010 23329690

72. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst Biol. 2010;59: 307–321. doi: 10.1093/sysbio/syq010 20525638

73. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest-HPC: Fast selection of best-fit models of protein evolution. Lect Notes Comput Sci (including Subser Lect Notes Artif Intell Lect Notes Bioinformatics). 2011;6586 LNCS: 177–184. 10.1007/978-3-642-21878-1_22

74. Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32: 268–274. doi: 10.1093/molbev/msu300 25371430

75. Shimodaira H, Hasegawa M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics. 2001;17: 1246–1247. doi: 10.1093/bioinformatics/17.12.1246 11751242

76. Lartillot N, Lepage T, Blanquart S. PhyloBayes 3: A Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009;25: 2286–2288. doi: 10.1093/bioinformatics/btp368 19535536

77. Letunic I, Bork P. Interactive Tree Of Life (iTOL): An online tool for phylogenetic tree display and annotation. Bioinformatics. 2007;23: 127–128. doi: 10.1093/bioinformatics/btl529 17050570

78. Sullivan MJ, Petty NK, Beatson SA. Easyfig: A genome comparison visualizer. Bioinformatics. 2011;27: 1009–1010. doi: 10.1093/bioinformatics/btr039 21278367

79. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9: 357–359. doi: 10.1038/nmeth.1923 22388286

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