Horizontal transfer, not duplication, drives the expansion of protein families in prokaryotes

PLoS Genetics

Volumn 7, Issue 1, 2011, Pages

  Treangen, Todd J ^a,b,c,d   Rocha, Eduardo P C ^a,b,c  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d Bldg 142   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN;

ARTICLE; BACILLUS; BACTERIAL GENOME; BACTERIAL STRAIN; BRADYRHIZOBIACEAE; CONTROLLED STUDY; ENTEROBACTERIACEAE; EVOLUTIONARY ADAPTATION; EVOLUTIONARY RATE; GENE DOSAGE; GENE DUPLICATION; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETIC LINE; GENETIC VARIABILITY; GENOME ANALYSIS; HELICOBACTER; HORIZONTAL GENE TRANSFER; MOLECULAR PHYLOGENY; NEISSERIA; NONHUMAN; PARALOGY; PROKARYOTE; PROPHAGE; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PSEUDOMONAS; SEQUENCE HOMOLOGY; STREPTOCOCCUS; SULFOLOBUS; TRANSIENT EXPRESSION; TRANSPOSON; BACTERIUM; BIOLOGY; GENETICS; MOLECULAR EVOLUTION; MULTIGENE FAMILY; PHYLOGENY;

BRADYRHIZOBIACEAE; ENTEROBACTERIACEAE; EUKARYOTA; HELICOBACTER; NEISSERIA; PROKARYOTA; PSEUDOMONAS; STREPTOCOCCUS; SULFOLOBUS;

BACILLUS; BACTERIA; BRADYRHIZOBIACEAE; COMPUTATIONAL BIOLOGY; ENTEROBACTERIACEAE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE TRANSFER, HORIZONTAL; GENOME, BACTERIAL; HELICOBACTER; MULTIGENE FAMILY; NEISSERIA; PHYLOGENY; PSEUDOMONAS; STREPTOCOCCUS; SULFOLOBUS;

EID: 79851505378     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001284     Document Type: Article

References (76)

1. McCutcheon JP, McDonald BR, Moran NA (2009) Origin of an alternative genetic code in the extremely small and GC-rich genome of a bacterial symbiont. PLoS Genet 5: e1000565 doi:10.1371/journal.pgen.1000565.
2. Schneiker S, Perlova O, Kaiser O, Gerth K, Alici A, et al. (2007) Complete genome sequence of the myxobacterium Sorangium cellulosum. Nat Biotechnol 25: 1281-1289.
3. Pasek S, Risler JL, Brezellec P (2006) The role of domain redundancy in genetic robustness against null mutations. J Mol Biol 362: 184-191.
4. Pereira-Leal JB, Levy ED, Kamp C, Teichmann SA (2007) Evolution of protein complexes by duplication of homomeric interactions. Genome Biol 8: R51.
5. Wagner A (2008) Gene duplications, robustness and evolutionary innovations. Bioessays 30: 367-373.
6. Francino MP (2005) An adaptive radiation model for the origin of new gene functions. Nat Genet 37: 573-577.
7. Kugelberg E, Kofoid E, Reams AB, Andersson DI, Roth JR (2006) Multiple pathways of selected gene amplification during adaptive mutation. Proc Natl Acad Sci U S A 103: 17319-17324.
8. Andersson DI, Hughes D (2009) Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 43: 167-195.
9. Conant GC, Wolfe KH (2008) Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet 9: 938-950.
10. Roth C, Rastogi S, Arvestad L, Dittmar K, Light S, et al. (2007) Evolution after gene duplication: models, mechanisms, sequences, systems, and organisms. J Exp Zoolog B Mol Dev Evol 308: 58-73.
11. Demuth JP, Hahn MW (2009) The life and death of gene families. Bioessays 31: 29-39.
12. Innan H, Kondrashov F (2010) The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97-108.
13. Alm E, Huang K, Arkin A (2006) The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLoS Comput Biol 2: e143 doi:10.1371/journal.pcbi.0020143.
14. Serres MH, Kerr AR, McCormack TJ, Riley M (2009) Evolution by leaps: gene duplication in bacteria. Biol Direct 4: 46.
15. Treangen TJ, Abraham AL, Touchon M, Rocha EP (2009) Genesis, effects and fates of repeats in prokaryotic genomes. FEMS Microbiol Rev 33: 539-571.
16. Cho NH, Kim HR, Lee JH, Kim SY, Kim J, et al. (2007) The Orientia tsutsugamushi genome reveals massive proliferation of conjugative type IV secretion system and host-cell interaction genes. Proc Natl Acad Sci U S A 104: 7981-7986.
17. Goldman BS, Nierman WC, Kaiser D, Slater SC, Durkin AS, et al. (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci U S A 103: 15200-15205.
18. McLeod MP, Warren RL, Hsiao WW, Araki N, Myhre M, et al. (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci U S A 103: 15582-15587.
19. Lindroos H, Vinnere O, Mira A, Repsilber D, Naslund K, et al. (2006) Genome rearrangements, deletions, and amplifications in the natural population of Bartonella henselae. J Bacteriol 188: 7426-7439.
20. Evlampiev K, Isambert H (2008) Conservation and topology of protein interaction networks under duplication-divergence evolution. Proc Natl Acad Sci U S A 105: 9863-9868.
21. Teichmann SA, Babu MM (2004) Gene regulatory network growth by duplication. Nat Genet 36: 492-496.
22. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299-304.
23. Lerat E, Daubin V, Ochman H, Moran NA (2005) Evolutionary origins of genomic repertoires in bacteria. PLoS Biol 3: e130 doi:10.1371/journal.pbio.0030130.
24. Gogarten JP, Doolittle WF, Lawrence JG (2002) Prokaryotic evolution in light of gene transfer. Mol Biol Evol 19: 2226-2238.
25. Tettelin H, Riley D, Cattuto C, Medini D (2008) Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11: 472-477.
26. Kunin V, Ouzounis CA (2003) The balance of driving forces during genome evolution in prokaryotes. Genome Res 13: 1589-1594.
27. Zhaxybayeva O, Gogarten JP, Charlebois RL, Doolittle WF, Papke RT (2006) Phylogenetic analyses of cyanobacterial genomes: quantification of horizontal gene transfer events. Genome Res 16: 1099-1108.
28. Dagan T, Artzy-Randrup Y, Martin W (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proc Natl Acad Sci U S A 105: 10039-10044.
29. Snel B, Bork P, Huynen MA (2002) Genomes in flux: the evolution of archaeal and proteobacterial gene content. Genome Res 12: 17-25.
30. Hooper SD, Berg OG (2003) Duplication is more common among laterally transferred genes than among indigenous genes. Genome Biol 4: R48.
31. Gevers D, Vandepoele K, Simillon C, Van de Peer Y (2004) Gene duplication and biased functional retention of paralogs in bacterial genomes. Trends Microbiol 12: 148-154.
32. Pushker R, Mira A, Rodriguez-Valera F (2004) Comparative genomics of gene-family size in closely related bacteria. Genome Biol 5: R27.
33. Pagel M, Meade A, Barker D (2004) Bayesian estimation of ancestral character states on phylogenies. Syst Biol 53: 673-684.
34. Wagner A (2006) Periodic extinctions of transposable elements in bacterial lineages: evidence from intragenomic variation in multiple genomes. Mol Biol Evol 23: 723-733.
35. Touchon M, Rocha EP (2007) Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 24: 969-981.
36. van Passel MW, Marri PR, Ochman H (2008) The emergence and fate of horizontally acquired genes in Escherichia coli. PLoS Comput Biol 4: e1000059 doi:10.1371/journal.pcbi.1000059.
37. Rocha EP (2008) Evolutionary patterns in prokaryotic genomes. Curr Opin Microbiol 11: 454-460.
38. Romero D, Palacios R (1997) Gene amplification and genomic plasticity in prokaryotes. Annu Rev Genet 31: 91-111.
39. Achaz G, Rocha EPC, Netter P, Coissac E (2002) Origin and fate of repeats in bacteria. Nucleic Acids Res 30: 2987-2994.
40. Howell-Adams B, Seifert HS (2000) Molecular models accounting for the gene conversion reactions mediating gonococcal pilin antigenic variation. Mol Microbiol 37: 1146-1158.
41. Aras RA, Kang J, Tschumi AI, Harasaki Y, Blaser MJ (2003) Extensive repetitive DNA facilitates prokaryotic genome plasticity. Proc Natl Acad Sci U S A 100: 13579-13584.
42. Falush D, Kraft C, Taylor NS, Correa P, Fox JG, et al. (2001) Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci U S A 98: 15056-15061.
43. Feil EJ, Holmes EC, Bessen DE, Chan MS, Day NP, et al. (2001) Recombination within natural populations of pathogenic bacteria: short- term empirical estimates and long-term phylogenetic consequences. Proc Natl Acad Sci U S A 98: 182-187.
44. Sharp PM, Li WH (1987) The codon Adaptation Index- a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15: 1281-1295.
45. Masuda T, Saito N, Tomita M, Ishihama Y (2009) Unbiased quantitation of Escherichia coli membrane proteome using phase transfer surfactants. Mol Cell Proteomics 8: 2770-2777.
46. Parmley JL, Hurst LD (2007) How common are intragene windows with KA>KS owing to purifying selection on synonymous mutations? J Mol Evol 64: 646-655.
47. Lawrence JG, Ochman H (1997) Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44: 383-397.
48. Vernikos GS, Thomson NR, Parkhill J (2007) Genetic flux over time in the Salmonella lineage. Genome Biol 8: R100.
49. Rocha EPC, Danchin A (2004) An analysis of determinants of protein substitution rates in Bacteria. Mol Biol Evol 21: 108-116.
50. Hu P, Janga SC, Babu M, Diaz-Mejia JJ, Butland G, et al. (2009) Global functional atlas of Escherichia coli encompassing previously uncharacterized proteins. PLoS Biol 7: e96 doi:10.1371/journal.pbio.1000096.
51. Martinez-Nunez MA, Perez-Rueda E, Gutierrez-Rios RM, Merino E (2010) New insights into the regulatory networks of paralogous genes in bacteria. Microbiology 156: 14-22.
52. Price MN, Dehal PS, Arkin AP (2008) Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol 9: R4.
53. Lercher MJ, Pal C (2008) Integration of horizontally transferred genes into regulatory interaction networks takes many million years. Mol Biol Evol 25: 559-567.
54. Cordero OX, Hogeweg P (2009) The impact of long-distance horizontal gene transfer on prokaryotic genome size. Proc Natl Acad Sci U S A 106: 21748-21753.
55. Sorek R, Zhu Y, Creevey CJ, Francino MP, Bork P, et al. (2007) Genome-wide experimental determination of barriers to horizontal gene transfer. Science 318: 1449-1452.
56. Vernikos G, Thomson N, Parkhill J (2007) Genetic flux over time in the Salmonella lineage. Genome Biology 8: R100.
57. Isambert H, Stein RR (2009) On the need for widespread horizontal gene transfers under genome size constraint. Biol Direct 4: 28.
58. Rocha EPC (2006) Inference and Analysis of the Relative Stability of Bacterial Chromosomes. Mol Biol Evol 23: 513-522.
59. Pal C, Papp B, Lercher MJ (2005) Adaptive evolution of bacterial metabolic networks by horizontal gene transfer. Nat Genet 37: 1372-1375.
60. Ochman H, Liu R, Rocha EP (2007) Erosion of interaction networks in reduced and degraded genomes. J Exp Zoolog B Mol Dev Evol 308: 97-103.
61. Wellner A, Lurie MN, Gophna U (2007) Complexity, connectivity, and duplicability as barriers to lateral gene transfer. Genome Biol 8: R156.
62. Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9: 605-618.
63. Derelle E, Ferraz C, Rombauts S, Rouze P, Worden AZ, et al. (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci U S A 103: 11647-11652.
64. Bowler C, Allen AE, Badger JH, Grimwood J, Jabbari K, et al. (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456: 239-244.
65. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
66. Enright AJ, Van Dongen S, Ouzounis CA (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30: 1575-1584.
67. Siguier P, Perochon J, Lestrade L, Mahillon J, Chandler M (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34: D32-36.
68. Fouts DE (2006) Phage_Finder: automated identification and classification of prophage regions in complete bacterial genome sequences. Nucleic Acids Res 34: 5839-5851.
69. Treangen TJ, Darling AE, Achaz G, Ragan MA, Messeguer X, et al. (2009) A novel heuristic for local multiple alignment of interspersed DNA repeats. IEEE/ACM Trans Comput Biol BioInf 6: 180-189.
70. Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
71. Rocha EP, Touchon M, Feil EJ (2006) Similar compositional biases are caused by very different mutational effects. Genome Res 16: 1537-1547.
72. Azad RK, Lawrence JG (2007) Detecting laterally transferred genes: use of entropic clustering methods and genome position. Nucleic Acids Res 35: 4629-4639.
73. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
74. Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18: 502-504.
75. Gascuel O (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Mol Biol Evol 14: 685-695.
76. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. CABIOS 13: 555-556.