Selection-Driven Gene Loss in Bacteria

English version České info

Gene loss by deletion is a common evolutionary process in bacteria, as exemplified by bacteria with small genomes that have evolved from bacteria with larger genomes by reductive processes. The driving force(s) for genome reduction remains unclear, and here we examined the hypothesis that gene loss is selected because carriage of superfluous genes confers a fitness cost to the bacterium. In the bacterium Salmonella enterica, we measured deletion rates at 11 chromosomal positions and the fitness effects of several spontaneous deletions. Deletion rates varied over 200-fold between different regions with the replication terminus region showing the highest rates. Approximately 25% of the examined deletions caused an increase in fitness under one or several growth conditions, and after serial passage of wild-type bacteria in rich medium for 1,000 generations we observed fixation of deletions that substantially increased bacterial fitness when reconstructed in a non-evolved bacterium. These results suggest that selection could be a significant driver of gene loss and reductive genome evolution.

Vyšlo v časopise: Selection-Driven Gene Loss in Bacteria. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002787
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002787

Souhrn

Zdroje

1. ZamenhofSEichhornHH 1967 Study of microbial evolution through loss of biosynthetic functions: establishment of “defective” mutants. Nature 216 456 458

2. DykhuizenD 1978 Selection for Tryptophan Auxotrophs of Escherichia coli in Glucose-Limited Chemostats as a Test of the Energy Conservation Hypothesis of Evolution. Evolution 32 125 150

3. KochAL 1983 The protein burden of lac operon products. J Mol Evol 19 455 462

4. BarrickJEYuDSYoonSHJeongHOhTK 2009 Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461 1243 1247

5. KhanAIDinhDMSchneiderDLenskiRECooperTF 2011 Negative epistasis between beneficial mutations in an evolving bacterial population. Science 332 1193 1196

6. DayWAJrFernandezREMaurelliAT 2001 Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect Immun 69 7471 7480

7. MaurelliAT 2007 Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett 267 1 8

8. MaurelliATFernandezREBlochCARodeCKFasanoA 1998 “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc Natl Acad Sci U S A 95 3943 3948

9. WernegreenJJMoranNA 1999 Evidence for genetic drift in endosymbionts (Buchnera): analyses of protein-coding genes. Mol Biol Evol 16 83 97

10. MoranNA 1996 Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A 93 2873 2878

11. AnderssonSGKurlandCG 1998 Reductive evolution of resident genomes. Trends Microbiol 6 263 268

12. MiraAOchmanHMoranNA 2001 Deletional bias and the evolution of bacterial genomes. Trends Genet 17 589 596

13. MoranNA 2002 Microbial minimalism: genome reduction in bacterial pathogens. Cell 108 583 586

14. MoranNA 2003 Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6 512 518

15. MoranNAPlagueGR 2004 Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14 627 633

16. MoyaAPeretoJGilRLatorreA 2008 Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9 218 229

17. KuoCHMoranNAOchmanH 2009 The consequences of genetic drift for bacterial genome complexity. Genome Res 19 1450 1454

18. McCutcheonJPMoranNA 2012 Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol 10 13 26

19. MoranNAMiraA 2001 The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. Genome Biol 2 RESEARCH0054

20. SilvaFJLatorreAMoyaA 2001 Genome size reduction through multiple events of gene disintegration in Buchnera APS. Trends Genet 17 615 618

21. MoranNBaumannP 1994 Phylogenetics of cytoplasmically inherited microorganisms of arthropods. Trends Ecol Evol 9 15 20

22. MoranNAWernegreenJJ 2000 Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 15 321 326

23. ShigenobuSWatanabeHHattoriMSakakiYIshikawaH 2000 Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407 81 86

24. DaleCWangBMoranNOchmanH 2003 Loss of DNA recombinational repair enzymes in the initial stages of genome degeneration. Mol Biol Evol 20 1188 1194

25. KlassonLAnderssonSG 2004 Evolution of minimal-gene-sets in host-dependent bacteria. Trends Microbiol 12 37 43

26. MoranNAMcCutcheonJPNakabachiA 2008 Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42 165 190

27. NilssonAIKoskiniemiSErikssonSKugelbergEHintonJC 2005 Bacterial genome size reduction by experimental evolution. Proc Natl Acad Sci U S A 102 12112 12116

28. DufresneAGarczarekLPartenskyF 2005 Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 6 R14

29. GiovannoniSJTrippHJGivanSPodarMVerginKL 2005 Genome streamlining in a cosmopolitan oceanic bacterium. Science 309 1242 1245

30. GiovannoniSJHayakawaDHTrippHJStinglUGivanSA 2008 The small genome of an abundant coastal ocean methylotroph. Environ Microbiol 10 1771 1782

31. ShenPHuangHV 1986 Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112 441 457

32. ChowSARaddingCM 1985 Ionic inhibition of formation of RecA nucleoprotein networks blocks homologous pairing. Proc Natl Acad Sci U S A 82 5646 5650

33. LindPATobinCBergOGKurlandCGAnderssonDI 2010 Compensatory gene amplification restores fitness after inter-species gene replacements. Mol Microbiol 75 1078 1089

34. EhrenbergMKurlandCG 1984 Costs of accuracy determined by a maximal growth rate constraint. Q Rev Biophys 17 45 82

35. KurlandCGCanbackBBergOG 2007 The origins of modern proteomes. Biochimie 89 1454 1463

36. AdkinsJNMottazHMNorbeckADGustinJKRueJ 2006 Analysis of the Salmonella typhimurium proteome through environmental response toward infectious conditions. Mol Cell Proteomics 5 1450 1461

37. MitchellJG 1991 The influence of cell size on marine bacterial motility and energetics. Microbial ecology 22 227 238

38. LouarnJMLouarnJFrancoisVPatteJ 1991 Analysis and possible role of hyperrecombination in the termination region of the Escherichia coli chromosome. J Bacteriol 173 5097 5104

39. LouarnJCornetFFrancoisVPatteJLouarnJM 1994 Hyperrecombination in the terminus region of the Escherichia coli chromosome: possible relation to nucleoid organization. J Bacteriol 176 7524 7531

40. LindroosHVinnereOMiraARepsilberDNaslundK 2006 Genome rearrangements, deletions, and amplifications in the natural population of Bartonella henselae. J Bacteriol 188 7426 7439

41. MillerJH 1992 A short course in bacterial genetics: Cold spring harbor press

42. DatsenkoKAWannerBL 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97 6640 6645

43. RiversSLMcNairnEBlascoFGiordanoGBoxerDH 1993 Molecular genetic analysis of the moa operon of Escherichia coli K-12 required for molybdenum cofactor biosynthesis. Mol Microbiol 8 1071 1081

44. LejeunePDanchinA 1990 Mutations in the bglY gene increase the frequency of spontaneous deletions in Escherichia coli K-12. Proc Natl Acad Sci U S A 87 360 363

45. Lea D.ECCA 1949 The distribution of the numbers of mutants in bacterial populations. J Genet 49 264 285

46. LuriaSEDelbruckM 1943 Mutations of Bacteria from Virus Sensitivity to Virus Resistance. Genetics 28 491 511