GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands
Classical population genetics models indicate that the efficiency of selection, and hence adaptation, depends on a number of non-selective factors, such as the size of a population or the intensity of recombination. In the last 10 years, evidence has accumulated that another mechanism called GC-Biased Gene Conversion (gBGC) can interfere with selection and even mimic its effects. This phenomenon, which arises from a particularity of the recombination machinery, was first thought to be restricted to sexual eukaryotic organisms. Here, we show that this mechanism probably exists in Bacteria and has a strong impact on their genome evolution. This discovery not only explains many previously unconnected features of bacterial genome evolution, but also highlights the importance of non-adaptive evolutionary processes in Bacteria.
Vyšlo v časopise:
GC-Content Evolution in Bacterial Genomes: The Biased Gene Conversion Hypothesis Expands. PLoS Genet 11(2): e32767. doi:10.1371/journal.pgen.1004941
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004941
Souhrn
Classical population genetics models indicate that the efficiency of selection, and hence adaptation, depends on a number of non-selective factors, such as the size of a population or the intensity of recombination. In the last 10 years, evidence has accumulated that another mechanism called GC-Biased Gene Conversion (gBGC) can interfere with selection and even mimic its effects. This phenomenon, which arises from a particularity of the recombination machinery, was first thought to be restricted to sexual eukaryotic organisms. Here, we show that this mechanism probably exists in Bacteria and has a strong impact on their genome evolution. This discovery not only explains many previously unconnected features of bacterial genome evolution, but also highlights the importance of non-adaptive evolutionary processes in Bacteria.
Zdroje
1. Doolittle WF (2013) Is junk DNA bunk? A critique of ENCODE. Proc Natl Acad Sci 110: 5294–5300. doi: 10.1073/pnas.1221376110 23479647
2. Bernardi G, Olofsson B, Filipski J, Zerial M, Salinas J, et al. (1985) The mosaic genome of warm-blooded vertebrates. Science 228: 953–958. 4001930
3. Sueoka N (1962) ON THE GENETIC BASIS OF VARIATION AND HETEROGENEITY OF DNA BASE COMPOSITION. Proc Natl Acad Sci 48: 582–592. 13918161
4. McCutcheon JP, Moran NA (2010) Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol 2: 708–718. doi: 10.1093/gbe/evq055 20829280
5. Pagani I, Liolios K, Jansson J, Chen I-MA, Smirnova T, et al. (2012) The Genomes OnLine Database (GOLD) v.4: status of genomic and metagenomic projects and their associated metadata. Nucleic Acids Res 40: D571–D579. doi: 10.1093/nar/gkr1100 22135293
6. Duret L, Galtier N (2009) Biased gene conversion and the evolution of mammalian genomic landscapes. Annu Rev Genomics Hum Genet 10: 285–311. doi: 10.1146/annurev-genom-082908-150001 19630562
7. Ratnakumar A, Mousset S, Glémin S, Berglund J, Galtier N, et al. (2010) Detecting positive selection within genomes: the problem of biased gene conversion. Philos Trans R Soc Lond B Biol Sci 365: 2571–2580. doi: 10.1098/rstb.2010.0007 20643747
8. Spencer CC, Deloukas P, Hunt S, Mullikin J, Myers S, et al. (2006). The influence of recombination on human genetic diversity. PLoS Genetics, 2:e148. doi: 10.1371/journal.pgen.0020148 17044736
9. Duret L, Arndt PF (2008) The Impact of Recombination on Nucleotide Substitutions in the Human Genome. PLoS Genet 4: e1000071. doi: 10.1371/journal.pgen.1000071 18464896
10. Webster MT, Hurst LD (2012) Direct and indirect consequences of meiotic recombination: implications for genome evolution. Trends Genet 28: 101–109. doi: 10.1016/j.tig.2011.11.002 22154475
11. Nagylaki T (1983) Evolution of a finite population under gene conversion. Proc Natl Acad Sci U S A 80: 6278–6281. 6578508
12. Galtier N, Duret L (2007) Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Trends Genet TIG 23: 273–277. doi: 10.1016/j.tig.2007.03.011 17418442
13. Galtier N, Duret L, Glémin S, Ranwez V (2009) GC-biased gene conversion promotes the fixation of deleterious amino acid changes in primates. Trends Genet TIG 25: 1–5. doi: 10.1016/j.tig.2008.10.011 19027980
14. Necşulea A, Popa A, Cooper DN, Stenson PD, Mouchiroud D, et al. (2011) Meiotic recombination favors the spreading of deleterious mutations in human populations. Hum Mutat 32: 198–206. doi: 10.1002/humu.21407 21120948
15. Mancera E, Bourgon R, Brozzi A, Huber W, Steinmetz LM (2008) High-resolution mapping of meiotic crossovers and non-crossovers in yeast. Nature 454: 479–485. doi: 10.1038/nature07135 18615017
16. Williams A, Geneovese G, Dyer T, Truax K, Jun G, et al. (2014) Non-crossover gene conversions show strong GC bias and unexpected clustering in humans. bioRxiv: 009175. doi: 10.1101/009175
17. Capra JA, Pollard KS (2011) Substitution patterns are GC-biased in divergent sequences across the metazoans. Genome Biol Evol 3: 516–527. doi: 10.1093/gbe/evr051 21670083
18. Escobar JS, Glémin S, Galtier N (2011) GC-biased gene conversion impacts ribosomal DNA evolution in vertebrates, angiosperms, and other eukaryotes. Mol Biol Evol 28: 2561–2575. doi: 10.1093/molbev/msr079 21444650
19. Pessia E, Popa A, Mousset S, Rezvoy C, Duret L, et al. (2012) Evidence for widespread GC-biased gene conversion in eukaryotes. Genome Biol Evol 4: 675–682. doi: 10.1093/gbe/evs052 22628461
20. Foerstner KU, von Mering C, Hooper SD, Bork P (2005) Environments shape the nucleotide composition of genomes. EMBO Rep 6: 1208–1213. doi: 10.1038/sj.embor.7400538 16200051
21. Sueoka N (1988) Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci U S A 85: 2653. 3357886
22. Hershberg R, Petrov DA (2010) Evidence That Mutation Is Universally Biased towards AT in Bacteria. PLoS Genet 6: e1001115. doi: 10.1371/journal.pgen.1001115 20838599
23. Hildebrand F, Meyer A, Eyre-Walker A (2010) Evidence of Selection upon Genomic GC-Content in Bacteria. PLoS Genet 6. doi: 10.1371/journal.pgen.1001107 20838593
24. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, et al. (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5: e1000344. doi: 10.1371/journal.pgen.1000344 19165319
25. Rocha EPC, Feil EJ (2010) Mutational Patterns Cannot Explain Genome Composition: Are There Any Neutral Sites in the Genomes of Bacteria? PLoS Genet 6: e1001104. doi: 10.1371/journal.pgen.1001104 20838590
26. Raghavan R, Kelkar YD, Ochman H (2012) A selective force favoring increased G+C content in bacterial genes. Proc Natl Acad Sci 109: 14504–14507. doi: 10.1073/pnas.1205683109 22908296
27. Penel S, Arigon A-M, Dufayard J-F, Sertier A-S, Daubin V, et al. (2009) Databases of homologous gene families for comparative genomics. BMC Bioinformatics 10: S3. doi: 10.1186/1471-2105-10-S6-S3 19534752
28. Bruen TC, Philippe H, Bryant D (2006) A Simple and Robust Statistical Test for Detecting the Presence of Recombination. Genetics 172: 2665–2681. doi: 10.1534/genetics.105.048975 16489234
29. Ussery DW, Kiil K, Lagesen K, Sicheritz-Pontén T, Bohlin J, et al. (2009) The genus burkholderia: analysis of 56 genomic sequences. Genome Dyn 6: 140–157. doi: 10.1159/000235768 19696499
30. Joseph SJ, Didelot X, Gandhi K, Dean D, Read TD (2011) Interplay of recombination and selection in the genomes of Chlamydia trachomatis. Biol Direct 6: 28. doi: 10.1186/1745-6150-6-28 21615910
31. Achtman M, Zurth K, Morelli G, Torrea G, Guiyoule A, et al. (1999) Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci 96: 14043–14048. doi: 10.1073/pnas.96.24.14043 10570195
32. Keim P, Johansson A, Wagner DM (2007) Molecular Epidemiology, Evolution, and Ecology of Francisella. Ann N Y Acad Sci 1105: 30–66. doi: 10.1196/annals.1409.011 17435120
33. Supply P, Marceau M, Mangenot S, Roche D, Rouanet C, et al. (2013) Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis. Nat Genet 45: 172–179. doi: 10.1038/ng.2517 23291586
34. Wattam AR, Williams KP, Snyder EE, Almeida NF Jr, Shukla M, et al. (2009) Analysis of ten Brucella genomes reveals evidence for horizontal gene transfer despite a preferred intracellular lifestyle. J Bacteriol 191: 3569–3579. doi: 10.1128/JB.01767-08 19346311
35. Whitaker RJ, Grogan DW, Taylor JW (2003) Geographic Barriers Isolate Endemic Populations of Hyperthermophilic Archaea. Science 301: 976–978. doi: 10.1126/science.1086909 12881573
36. Reno ML, Held NL, Fields CJ, Burke PV, Whitaker RJ (2009) Biogeography of the Sulfolobus islandicus pan-genome. Proc Natl Acad Sci 106: 8605–8610. doi: 10.1073/pnas.0808945106 19435847
37. McVean GA, Charlesworth B (2000) The effects of Hill-Robertson interference between weakly selected mutations on patterns of molecular evolution and variation. Genetics 155: 929–944. 10835411
38. Hershberg R, Petrov DA (2009) General Rules for Optimal Codon Choice. PLoS Genet 5: e1000556. doi: 10.1371/journal.pgen.1000556 19593368
39. Wang B, Shao Z-Q, Xu Y, Liu J, Liu Y, et al. (2011) Optimal Codon Identities in Bacteria: Implications from the Conflicting Results of Two Different Methods. PLoS ONE 6: e22714. doi: 10.1371/journal.pone.0022714 21829489
40. Hershberg R, Petrov DA (2012) On the Limitations of Using Ribosomal Genes as References for the Study of Codon Usage: A Rebuttal. PLoS ONE 7: e49060. doi: 10.1371/journal.pone.0049060 23284622
41. Didelot X, Lawson D, Darling A, Falush D (2010) Inference of Homologous Recombination in Bacteria Using Whole Genome Sequences. Genetics 186: 1435–1449. doi: 10.1534/genetics.110.120121 20923983
42. Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851–861. doi: 10.1038/nature06258 17943122
43. Balbi KJ, Rocha EPC, Feil EJ (2009) The Temporal Dynamics of Slightly Deleterious Mutations in Escherichia coli and Shigella spp. Mol Biol Evol 26: 345–355. doi: 10.1093/molbev/msn252 18984902
44. Cole F, Baudat F, Grey C, Keeney S, de Massy B, et al. (2014) Mouse tetrad analysis provides insights into recombination mechanisms and hotspot evolutionary dynamics. Nat Genet 46: 1072–1080. doi: 10.1038/ng.3068 25151354
45. Munch K, Mailund T, Dutheil JY, Schierup MH (2014) A fine-scale recombination map of the human-chimpanzee ancestor reveals faster change in humans than in chimpanzees and a strong impact of GC-biased gene conversion. Genome Res 24: 467–474. doi: 10.1101/gr.158469.113 24190946
46. Moran NA (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108: 583–586. 11893328
47. Lynch M (2010) Rate, molecular spectrum, and consequences of human mutation. Proc Natl Acad Sci 107: 961–968. doi: 10.1073/pnas.0912629107 20080596
48. Lesecque Y, Mouchiroud D, Duret L (2013) GC-Biased Gene Conversion in Yeast Is Specifically Associated with Crossovers: Molecular Mechanisms and Evolutionary Significance. Mol Biol Evol 30: 1409–1419. doi: 10.1093/molbev/mst056 23505044
49. Glémin S (2010) Surprising fitness consequences of GC-biased gene conversion: I. Mutation load and inbreeding depression. Genetics 185: 939–959. doi: 10.1534/genetics.110.116368 20421602
50. Suerbaum S, Smith JM, Bapumia K, Morelli G, Smith NH, et al. (1998) Free recombination within Helicobacter pylori. Proc Natl Acad Sci 95: 12619–12624. doi: 10.1073/pnas.95.21.12619 9770535
51. 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 98: 15056–15061. doi: 10.1073/pnas.251396098 11742075
52. Lin Z, Nei M, Ma H (2007) The origins and early evolution of DNA mismatch repair genes-multiple horizontal gene transfers and co-evolution. Nucleic Acids Res 35: 7591–7603. doi: 10.1093/nar/gkm921 17965091
53. Retchless AC, Lawrence JG (2007) Temporal fragmentation of speciation in bacteria. Science 317: 1093–1096. doi: 10.1126/science.1144876 17717188
54. Daubin V, Lerat E, Perrière G (2003) The source of laterally transferred genes in bacterial genomes. Genome Biol 4: R57. doi: 10.1186/gb-2003-4-9-r57 12952536
55. Daubin V, Ochman H (2004) Bacterial Genomes as New Gene Homes: The Genealogy of ORFans in E. coli. Genome Res 14: 1036–1042. doi: 10.1101/gr.2231904 15173110
56. Gouy M, Gautier C, Attimonelli M, Lanave C, di Paola G (1985) ACNUC—a portable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. Comput Appl Biosci CABIOS 1: 167–172. 3880341
57. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113. doi: 10.1186/1471-2105-5-113 15318951
58. Jakobsen IB, Easteal S (1996) A program for calculating and displaying compatibility matrices as an aid in determining reticulate evolution in molecular sequences. Comput Appl Biosci CABIOS 12: 291–295. 8902355
59. Smith JM (1992) Analyzing the mosaic structure of genes. J Mol Evol 34: 126–129. 1556748
60. Sawyer S (1989) Statistical tests for detecting gene conversion. Mol Biol Evol 6: 526–538. 2677599
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2015 Číslo 2
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Genomic Selection and Association Mapping in Rice (): Effect of Trait Genetic Architecture, Training Population Composition, Marker Number and Statistical Model on Accuracy of Rice Genomic Selection in Elite, Tropical Rice Breeding Lines
- Discovery of Transcription Factors and Regulatory Regions Driving Tumor Development by ATAC-seq and FAIRE-seq Open Chromatin Profiling
- Evolutionary Signatures amongst Disease Genes Permit Novel Methods for Gene Prioritization and Construction of Informative Gene-Based Networks
- Proteotoxic Stress Induces Phosphorylation of p62/SQSTM1 by ULK1 to Regulate Selective Autophagic Clearance of Protein Aggregates