#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A spectrum of verticality across genes


Autoři: Falk S. P. Nagies aff001;  Julia Brueckner aff001;  Fernando D. K. Tria aff001;  William F. Martin aff001
Působiště autorů: Institute for Molecular Evolution, Heinrich Heine University Düsseldorf, Düsseldorf, Germany aff001
Vyšlo v časopise: A spectrum of verticality across genes. PLoS Genet 16(11): e32767. doi:10.1371/journal.pgen.1009200
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009200

Souhrn

Lateral gene transfer (LGT) has impacted prokaryotic genome evolution, yet the extent to which LGT compromises vertical evolution across individual genes and individual phyla is unknown, as are the factors that govern LGT frequency across genes. Estimating LGT frequency from tree comparisons is problematic when thousands of genomes are compared, because LGT becomes difficult to distinguish from phylogenetic artefacts. Here we report quantitative estimates for verticality across all genes and genomes, leveraging a well-known property of phylogenetic inference: phylogeny works best at the tips of trees. From terminal (tip) phylum level relationships, we calculate the verticality for 19,050,992 genes from 101,422 clusters in 5,655 prokaryotic genomes and rank them by their verticality. Among functional classes, translation, followed by nucleotide and cofactor biosynthesis, and DNA replication and repair are the most vertical. The most vertically evolving lineages are those rich in ecological specialists such as Acidithiobacilli, Chlamydiae, Chlorobi and Methanococcales. Lineages most affected by LGT are the α-, β-, γ-, and δ- classes of Proteobacteria and the Firmicutes. The 2,587 eukaryotic clusters in our sample having prokaryotic homologues fail to reject eukaryotic monophyly using the likelihood ratio test. The low verticality of α-proteobacterial and cyanobacterial genomes requires only three partners—an archaeal host, a mitochondrial symbiont, and a plastid ancestor—each with mosaic chromosomes, to directly account for the prokaryotic origin of eukaryotic genes. In terms of phylogeny, the 100 most vertically evolving prokaryotic genes are neither representative nor predictive for the remaining 97% of an average genome. In search of factors that govern LGT frequency, we find a simple but natural principle: Verticality correlates strongly with gene distribution density, LGT being least likely for intruding genes that must replace a preexisting homologue in recipient chromosomes. LGT is most likely for novel genetic material, intruding genes that encounter no competing copy.

Klíčová slova:

Eukaryota – Evolutionary genetics – Genomics – Microbial evolution – Phylogenetic analysis – Phylogenetics – Prokaryotic cells – Sequence alignment


Zdroje

1. McDaniel LD, Young E, Delaney J, Ruhnau F, Ritchie KB, Paul JH. High frequency of horizontal gene transfer in the oceans. Science 2010;330(6000):50. doi: 10.1126/science.1192243 20929803

2. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000;405(6784):299–304. doi: 10.1038/35012500 10830951

3. Popa O, Dagan T. Trends and barriers to lateral gene transfer in prokaryotes. Curr Opin Microbiol 2011;14(5):615–623. doi: 10.1016/j.mib.2011.07.027 21856213

4. Rasko DA, Rosovitz MJ, Myers GSA, Mongodin EF, Fricke WF, Gajer P, et al. The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 2008;190(20):6881–6893. doi: 10.1128/JB.00619-08 18676672

5. Lukjancenko O, Wassenaar TM, Ussery DW. Comparison of 61 sequenced Escherichia coli genomes. Microb Ecol 2010;60(4):708–720. doi: 10.1007/s00248-010-9717-3 20623278

6. Hansmann S, Martin W. Phylogeny of 33 ribosomal and six other proteins encoded in an ancient gene cluster that is conserved across prokaryotic genomes: influence of excluding poorly alignable sites from analysis. Int J Syst Evol Microbiol 2000;50 Pt 4:1655–1663 doi: 10.1099/00207713-50-4-1655 10939673

7. Charlebois RL, Doolittle WF. Computing prokaryotic gene ubiquity: rescuing the core from extinction. Genome Res 2004;14(12):2469–2477. doi: 10.1101/gr.3024704 15574825

8. Ciccarelli FD, Doerks T, von Mering C, Creevey CJ, Snel B, Bork P. Toward automatic reconstruction of a highly resolved tree of life. Science 2006;311(5765):1283–1287. doi: 10.1126/science.1123061 16513982

9. Dagan T, Martin W. The tree of one percent. Genome Biol 2006;7(10):118. doi: 10.1186/gb-2006-7-10-118 17081279

10. Koonin EV, Wolf YI, Puigbò P. The phylogenetic forest and the quest for the elusive tree of life. Cold Spring Harb Symp Quant Biol 2009;74:205–213. doi: 10.1101/sqb.2009.74.006 19687142

11. Dagan T, Artzy-Randrup Y, Martin W. Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Natl Acad Sci U S A 2008;105(29):10039–10044. doi: 10.1073/pnas.0800679105 18632554

12. Ku C, Martin WF. A natural barrier to lateral gene transfer from prokaryotes to eukaryotes revealed from genomes: the 70% rule. BMC Biol 2016;14(1):89. doi: 10.1186/s12915-016-0315-9 27751184

13. Sorek R, Zhu Y, Creevey CJ, Francino MP, Bork P, Rubin EM. Genome-wide experimental determination of barriers to horizontal gene transfer. Science 2007;318(5855):1449–1452. doi: 10.1126/science.1147112 17947550

14. Pál C, Papp B, Lercher MJ. Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 2005;37(12):1372–1375. doi: 10.1038/ng1686 16311593

15. Lercher MJ, Pál C. Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol Biol Evol 2008;25(3):559–567. doi: 10.1093/molbev/msm283 18158322

16. Chen W-H, Trachana K, Lercher MJ, Bork P. Younger genes are less likely to be essential than older genes, and duplicates are less likely to be essential than singletons of the same age. Mol Biol Evol 2012;29(7):1703–1706. doi: 10.1093/molbev/mss014 22319151

17. Dilthey A, Lercher MJ. Horizontally transferred genes cluster spatially and metabolically. Biol Direct 2015;10:72. doi: 10.1186/s13062-015-0102-5 26690249

18. Grassi L, Caselle M, Lercher MJ, Lagomarsino MC. Horizontal gene transfers as metagenomic gene duplications. Mol Biosyst 2012;8(3):790–795. doi: 10.1039/c2mb05330f 22218456

19. Nelson-Sathi S, Dagan T, Landan G, Janssen A, Steel M, McInerney JO, et al. Acquisition of 1,000 eubacterial genes physiologically transformed a methanogen at the origin of Haloarchaea. Proc Natl Acad Sci U S A 2012;109(50):20537–20542. doi: 10.1073/pnas.1209119109 23184964

20. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007;315(5819):1709–1712. doi: 10.1126/science.1138140 17379808

21. Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A 2015;112(27):E3574–E3581. doi: 10.1073/pnas.1501049112 26100894

22. Brockhurst MA, Harrison E, Hall JPJ, Richards T, McNally A, MacLean C. The ecology and evolution of pangenomes. Curr Biol 2019;29(20):R1094–R1103. doi: 10.1016/j.cub.2019.08.012 31639358

23. Croll D, McDonald BA. The accessory genome as a cradle for adaptive evolution in pathogens. PLoS Pathog 2012;8(4):e1002608. doi: 10.1371/journal.ppat.1002608 22570606

24. McInerney JO, McNally A, O’Connell MJ. Why prokaryotes have pangenomes. Nat Microbiol 2017;2:17040. doi: 10.1038/nmicrobiol.2017.40 28350002

25. Vernikos G, Medini D, Riley DR, Tettelin H. Ten years of pan-genome analyses. Curr Opin Microbiol 2015;23:148–154. doi: 10.1016/j.mib.2014.11.016 25483351

26. Chatton E. Pansporella perplexa. Amoebien a spores protégées parasite des daphnies. Réflexions sur la biologie et la phylogénie des protozoaires. Ann Sci Nat Zool 1925;8:5–85.

27. Creevey CJ, Fitzpatrick DA, Philip GK, Kinsella RJ, O’Connell MJ, Pentony MM, et al. Does a tree-like phylogeny only exist at the tips in the prokaryotes? Proc Biol Sci 2004;271(1557):2551–2558. doi: 10.1098/rspb.2004.2864 15615680

28. Semple C, Steel MA. Phylogenetics. Reprinted. Oxford: Oxford Univ. Press; 2009. (Oxford lecture series in mathematics and its applications; vol 24).

29. McPherson RA. The Numbers Universe: An outline of the dirac/eddington numbers as scaling factors for fractal, black hole universes. Electronic Journal of Theoretical Physics 2008;5(18).

30. Nakamura Y, Itoh T, Matsuda H, Gojobori T. Biased biological functions of horizontally transferred genes in prokaryotic genomes. Nat Genet 2004;36(7):760–766. doi: 10.1038/ng1381 15208628

31. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454 3447015

32. Landan G, Graur D. Heads or tails: a simple reliability check for multiple sequence alignments. Mol Biol Evol 2007;24(6):1380–1383. doi: 10.1093/molbev/msm060 17387100

33. Criscuolo A. morePhyML: improving the phylogenetic tree space exploration with PhyML 3. Mol Phylogenet Evol 2011;61(3):944–948. doi: 10.1016/j.ympev.2011.08.029 21925283

34. Treangen TJ, Rocha EPC. Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes. PLoS Genet 2011;7(1):e1001284. doi: 10.1371/journal.pgen.1001284 21298028

35. Tria FDK, Brückner J, Skejo J, Xavier JC, Zimorski V, Gould SB, et al. Gene duplications trace mitochondria to the onset of eukaryote complexity; 2019. (vol 176) bioRxiv. doi: 10.1101/781211

36. Szöllősi GJ, Davín AA, Tannier E, Daubin V, Boussau B. Genome-scale phylogenetic analysis finds extensive gene transfer among fungi. Philos Trans R Soc Lond B, Biol Sci 2015;370(1678):20140335. doi: 10.1098/rstb.2014.0335 26323765

37. Jain R, Rivera MC, Lake JA. Horizontal gene transfer among genomes: the complexity hypothesis. Proc Natl Acad Sci U S A 1999;96(7):3801–3806. doi: 10.1073/pnas.96.7.3801 10097118

38. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016;2(1):vew007. doi: 10.1093/ve/vew007 27774300

39. Niehus R, Mitri S, Fletcher AG, Foster KR. Migration and horizontal gene transfer divide microbial genomes into multiple niches. Nat Commun 2015;6:8924. doi: 10.1038/ncomms9924 26592443

40. Nei M. Molecular evolutionary genetics. New York: Columbia University Press; 1987.

41. Aziz RK, Breitbart M, Edwards RA. Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 2010;38(13):4207–4217. doi: 10.1093/nar/gkq140 20215432

42. Nevers P, Saedler H. Transposable genetic elements as agents of gene instability and chromosomal rearrangements. Nature 1977;268(5616):109–115. doi: 10.1038/268109a0 339095

43. Goremykin VV, Hansmann S, Martin WF. Evolutionary analysis of 58 proteins encoded in six completely sequenced chloroplast genomes: Revised molecular estimates of two seed plant divergence times. Pl Syst Evol 1997;206(1–4):337–351.

44. Martin W, Stoebe B, Goremykin V, Hapsmann S, Hasegawa M, Kowallik KV. Gene transfer to the nucleus and the evolution of chloroplasts. Nature 1998;393(6681):162–165. doi: 10.1038/30234 11560168

45. Imachi H, Nobu MK, Nakahara N, Morono Y, Ogawara M, Takaki Y, et al. Isolation of an archaeon at the prokaryote-eukaryote interface. Nature 2020;577(7791):519–525. doi: 10.1038/s41586-019-1916-6 31942073

46. Fan L, Wu D, Goremykin V, Xiao J, Xu Y, Garg S, et al. Phylogenetic analyses with systematic taxon sampling show that mitochondria branch within alphaproteobacteria. Nat Ecol Evol 2020. doi: 10.1038/s41559-020-1239-x 32661403

47. Lang BF, Burger G, O’Kelly CJ, Cedergren R, Golding GB, Lemieux C, et al. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 1997;387(6632):493–497. doi: 10.1038/387493a0 9168110

48. Tian R-M, Cai L, Zhang W-P, Cao H-L, Qian P-Y. Rare Events of Intragenus and Intraspecies Horizontal Transfer of the 16S rRNA Gene. Genome Biol Evol 2015;7(8):2310–2320. doi: 10.1093/gbe/evv143 26220935

49. Schönheit P, Buckel W, Martin WF. On the origin of heterotrophy. Trends Microbiol 2016;24(1):12–25. doi: 10.1016/j.tim.2015.10.003 26578093

50. Husnik F, Keeling PJ. The fate of obligate endosymbionts: reduction, integration, or extinction. Curr Opin Genet Dev 2019;58–59:1–8. doi: 10.1016/j.gde.2019.07.014 31470232

51. Tamames J, Gil R, Latorre A, Peretó J, Silva FJ, Moya A. The frontier between cell and organelle: genome analysis of Candidatus Carsonella ruddii. BMC Evol Biol 2007;7:181. doi: 10.1186/1471-2148-7-181 17908294

52. Podar M, Anderson I, Makarova KS, Elkins JG, Ivanova N, Wall MA, et al. A genomic analysis of the archaeal system Ignicoccus hospitalis-Nanoarchaeum equitans. Genome Biol 2008;9(11):R158. doi: 10.1186/gb-2008-9-11-r158 19000309

53. Anderson I, Djao ODN, Misra M, Chertkov O, Nolan M, Lucas S, et al. Complete genome sequence of Methanothermus fervidus type strain (V24S). Stand Genomic Sci 2010;3(3):315–324. doi: 10.4056/sigs.1283367 21304736

54. Gabaldón T. Relative timing of mitochondrial endosymbiosis and the “pre-mitochondrial symbioses” hypothesis. IUBMB Life 2018;70(12):1188–1196. doi: 10.1002/iub.1950 30358047

55. Kapust N, Nelson-Sathi S, Schönfeld B, Hazkani-Covo E, Bryant D, Lockhart PJ, et al. Failure to recover major events of gene flux in real biological data due to method misapplication. Genome Biol Evol 2018;10(5):1198–1209. doi: 10.1093/gbe/evy080 29718211

56. Martin W, Rujan T, Richly E, Hansen A, Cornelsen S, Lins T, et al. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc Natl Acad Sci U S A 2002;99(19):12246–12251. doi: 10.1073/pnas.182432999 12218172

57. Ku C, Nelson-Sathi S, Roettger M, Garg S, Hazkani-Covo E, Martin WF. Endosymbiotic gene transfer from prokaryotic pangenomes: Inherited chimerism in eukaryotes. Proc Natl Acad Sci U S A 2015;112(33):10139–10146. doi: 10.1073/pnas.1421385112 25733873

58. Martin WF, Garg S, Zimorski V. Endosymbiotic theories for eukaryote origin. Philos Trans R Soc Lond B, Biol Sci 2015;370(1678):20140330. doi: 10.1098/rstb.2014.0330 26323761

59. Hittinger CT, Carroll SB. Gene duplication and the adaptive evolution of a classic genetic switch. Nature 2007;449(7163):677–681. doi: 10.1038/nature06151 17928853

60. van de Peer Y, Maere S, Meyer A. The evolutionary significance of ancient genome duplications. Nat Rev Genet 2009;10(10):725–732. doi: 10.1038/nrg2600 19652647

61. Maier U-G, Zauner S, Woehle C, Bolte K, Hempel F, Allen JF, et al. Massively convergent evolution for ribosomal protein gene content in plastid and mitochondrial genomes. Genome Biol Evol 2013;5(12):2318–2329. doi: 10.1093/gbe/evt181 24259312

62. Allen JF, Martin WF. Why have organelles retained genomes? Cell Syst 2016;2(2):70–72. doi: 10.1016/j.cels.2016.02.007 27135161

63. Vos M, Hesselman MC, Te Beek TA, van Passel MWJ, Eyre-Walker A. Rates of lateral gene transfer in prokaryotes: High but why? Trends Microbiol 2015; 23(10):598–605. doi: 10.1016/j.tim.2015.07.006 26433693

64. Sela I, Wolf YI, Koonin EV. Theory of prokaryotic genome evolution. Proc Natl Acad Sci U S A 2016;113(41):11399–11407. doi: 10.1073/pnas.1614083113 27702904

65. Martin W. Mosaic bacterial chromosomes: a challenge en route to a tree of genomes. Bioessays 1999;21(2):99–104. doi: 10.1002/(SICI)1521-1878(199902)21:2<99::AID-BIES3>3.0.CO;2-B 10193183

66. Puigbò P, Wolf YI, Koonin EV. Genome-wide comparative analysis of phylogenetic trees: The prokaryotic forest of life. Methods Mol Biol 2019;1910:241–269. doi: 10.1007/978-1-4939-9074-0_8 31278667

67. Wright ES, Baum DA. Exclusivity offers a sound yet practical species criterion for bacteria despite abundant gene flow. BMC Genomics 2018;19(1):724. doi: 10.1186/s12864-018-5099-6 30285620

68. O’Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, et al. Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Res 2016;44(D1):D733–D745 doi: 10.1093/nar/gkv1189 26553804

69. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of Molecular Biology 1990;215(3):403–10. doi: 10.1016/S0022-2836(05)80360-2 2231712

70. Rice P, Longden I, Bleasby A. EMBOSS: the European molecular biology open software suite. Trends Genet. 2000;(16):276–277. doi: 10.1016/s0168-9525(00)02024-2 10827456

71. Enright AJ, van Dongen S, Ouzounis CA. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 2002;30(7):1575–1584. doi: 10.1093/nar/30.7.1575 11917018

72. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013;30(4):772–780. doi: 10.1093/molbev/mst010 23329690

73. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30(9):1312–1313. doi: 10.1093/bioinformatics/btu033 24451623

74. Tria FDK, Landan G, Dagan T. Phylogenetic rooting using minimal ancestor deviation. Nat Ecol Evol 2017;1:193. doi: 10.1038/s41559-017-0193 29388565

75. Nguyen L-T, 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(1):268–274. doi: 10.1093/molbev/msu300 25371430

76. Junier T, Zdobnov EM. The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics 2010;26(13):1669–1670. doi: 10.1093/bioinformatics/btq243 20472542

77. Huerta-Cepas J, Serra F, Bork P. ETE 3: Reconstruction, analysis, and visualization of phylogenomic data. Mol Biol Evol 2016;33(6):1635–1638. doi: 10.1093/molbev/msw046 26921390

78. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 2016;44(D1):D457–D462 doi: 10.1093/nar/gkv1070 26476454

79. Kishino H, Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. Journal of molecular evolution 1989;29(2):170–9. doi: 10.1007/BF02100115 2509717

80. Shimodaira H, Hasegawa M. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 1999;16(8):1114–1116 doi: 10.1093/oxfordjournals.molbev.a026201

81. Shimodaira H. An approximately unbiased test of phylogenetic tree selection. Systematic biology 2002;51(3):492–508. doi: 10.1080/10635150290069913 12079646

82. Price MN, Dehal PS, Arkin AP. FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 2010;5(3):e9490. doi: 10.1371/journal.pone.0009490 20224823

83. Havlicek LL, Peterson NL. Robustness of the pearson correlation against violations of assumptions. Percept Mot Skills 1976;43(3_suppl):1319–1334 doi: 10.2466/pms.1976.43.3f.1319


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 11
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autoři: MUDr. Tomáš Ürge, PhD.

Střevní příprava před kolonoskopií
Autoři: MUDr. Klára Kmochová, Ph.D.

Závislosti moderní doby – digitální závislosti a hypnotika
Autoři: MUDr. Vladimír Kmoch

Aktuální možnosti diagnostiky a léčby AML a MDS nízkého rizika
Autoři: MUDr. Natália Podstavková

Jak diagnostikovat a efektivně léčit CHOPN v roce 2024
Autoři: doc. MUDr. Vladimír Koblížek, Ph.D.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#