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Patterns of Evolutionary Conservation of Essential Genes Correlate with Their Compensability


Essential genes code for fundamental cellular functions required for the viability of an organism. For this reason, essential genes are often highly conserved across organisms. However, this is not always the case: orthologues of genes that are essential in one organism are sometimes not essential in other organisms or are absent from their genomes. This suggests that, in the course of evolution, essential genes can be rendered nonessential. How can a gene become non-essential? Here we used genetic manipulation to deplete the products of 26 different essential genes in Escherichia coli. This depletion results in a lethal phenotype, which could often be rescued by the overexpression of a non-homologous, non-essential gene, most likely through replacement of the essential function. We also show that, in a smaller number of cases, the essential genes can be fully deleted from the genome, suggesting that complete functional replacement is possible. Finally, we show that essential genes whose function can be replaced in the laboratory are more likely to be non-essential or not present in other taxa. These results are consistent with the notion that patterns of evolutionary conservation of essential genes are influenced by their compensability—that is, by how easily they can be functionally replaced, for example through increased expression of other genes.


Vyšlo v časopise: Patterns of Evolutionary Conservation of Essential Genes Correlate with Their Compensability. PLoS Genet 8(6): e32767. doi:10.1371/journal.pgen.1002803
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002803

Souhrn

Essential genes code for fundamental cellular functions required for the viability of an organism. For this reason, essential genes are often highly conserved across organisms. However, this is not always the case: orthologues of genes that are essential in one organism are sometimes not essential in other organisms or are absent from their genomes. This suggests that, in the course of evolution, essential genes can be rendered nonessential. How can a gene become non-essential? Here we used genetic manipulation to deplete the products of 26 different essential genes in Escherichia coli. This depletion results in a lethal phenotype, which could often be rescued by the overexpression of a non-homologous, non-essential gene, most likely through replacement of the essential function. We also show that, in a smaller number of cases, the essential genes can be fully deleted from the genome, suggesting that complete functional replacement is possible. Finally, we show that essential genes whose function can be replaced in the laboratory are more likely to be non-essential or not present in other taxa. These results are consistent with the notion that patterns of evolutionary conservation of essential genes are influenced by their compensability—that is, by how easily they can be functionally replaced, for example through increased expression of other genes.


Zdroje

1. BabaTAraTHasegawaMTakaiYOkumuraY 2006 Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Molecular Systems Biology 2 2006.0008

2. KatoJIHashimotoM 2007 Construction of consecutive deletions of the Escherichia coli chromosome. Molecular Systems Biology 3 132

3. ChristenBAbeliukECollierJMKalogerakiVSPassarelliB 2011 The essential genome of a bacterium. Molecular Systems Biology 7

4. GlassJIAssad-GarciaNAlperovichNYoosephSLewisMR 2006 Essential genes of a minimal bacterium. Proceedings of the National Academy of Sciences of the United States of America 103 425 430

5. KobayashiKEhrlichSDAlbertiniAAmatiGAndersenKK 2003 Essential Bacillus subtilis genes. Proceedings of the National Academy of Sciences of the United States of America 100 4678 4683

6. de BerardinisVVallenetDCastelliVBesnardMPinetA 2008 A complete collection of single-gene deletion mutants of Acinetobacter baylyi ADP1. Molecular Systems Biology 4 174

7. LangridgeGCPhanMDTurnerDJPerkinsTTPartsL 2009 Simultaneous assay of every Salmonella Typhi gene using one million transposon mutants. Genome Research 19 2308 2316

8. van OpijnenTBodiKLCamilliA 2009 Tn-seq: high-throughput parallel sequencing for fitness and genetic interaction studies in microorganisms. Nature Methods 6 767 U721

9. GallagherLARamageEJacobstMAKaulRBrittnacherM 2007 A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proceedings of the National Academy of Sciences of the United States of America 104 1009 1014

10. FrenchCTLaoPLoraineAEMatthewsBTYuHL 2008 Large-scale transposon mutagenesis of Mycoplasma pulmonis. Molecular Microbiology 69 67 76

11. ChaudhuriRRAllenAGOwenPJShalomGStoneK 2009 Comprehensive identification of essential Staphylococcus aureus genes using Transposon-Mediated Differential Hybridisation (TMDH). Bmc Genomics 10

12. JordanIKRogozinIBWolfYIKooninEV 2002 Essential genes are more evolutionarily conserved than are nonessential genes in bacteria. Genome Research 12 962 968

13. GerdesSYScholleMDCampbellJWBalazsiGRavaszE 2003 Experimental determination and system level analysis of essential genes in Escherichia coli MG1655. Journal of Bacteriology 185 5673 5684

14. RochaEPCDanchinA 2004 An analysis of determinants of amino acids substitution rates in bacterial proteins. Molecular Biology and Evolution 21 108 116

15. SilanderOKAckermannM 2009 The constancy of gene conservation across divergent bacterial orders. BMC Research Notes 2 2

16. KooninEV 2003 Comparative genomics, minimal gene-sets and the last universal common ancestor. Nature Reviews Microbiology 1 127 136

17. GeisslerBElrahebDMargolinW 2003 A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 100 4197 4202

18. CardinaleCJWashburnRSTadigotlaVRBrownLMGottesmanME 2008 Termination factor Rho and its cofactors NusA and NusG silence foreign DNA in E-coli. Science 320 935 938

19. AlbaBMZhongHJPelayoJCGrossCA 2001 degS (hhoB) is an essential Escherichia coli gene whose indispensable function is to provide sigma(E) activity. Molecular Microbiology 40 1323 1333

20. CostaCSPettinariMJMendezBSAntonDN 2003 Null mutations in the essential gene yrfF (mucM) are not lethal in rcsB, yojN or rcsC strains of Salmonella enterica serovar Typhimurium. Fems Microbiology Letters 222 25 32

21. PeistRKochABolekPSewitzSKolbusT 1997 Characterization of the aes gene of Escherichia coli encoding an enzyme with esterase activity. Journal of Bacteriology 179 7679 7686

22. SerresMHRileyM 2000 MultiFun, a multifunctional classification scheme for Escherichia coli K-12 gene products. Microb Comp Genomics 5 205 222

23. SakaKTadenumaMNakadeSTanakaNSugawaraH 2005 A complete set of Escherichia coli open reading frames in mobile plasmids facilitating genetic studies. DNA Research 12 63 68

24. FirthAEPatrickWM 2005 Statistics of protein library construction. Bioinformatics 21 3314 3315

25. HandfordJIIzeBBuchananGButlandGPGreenblattJ 2009 Conserved Network of Proteins Essential for Bacterial Viability. Journal of Bacteriology 191 4732 4749

26. TouatiDJacquesMTardatBBouchardLDespiedS 1995 Lethal Oxidative Damage and Mutagenesis Are Generated by Iron in Delta-Fur Mutants of Escherichia-Coli - Protective Role of Superoxide-Dismutase. Journal of Bacteriology 177 2305 2314

27. McCoolJDLongEPetrosinoJFSandlerHARosenbergSM 2004 Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Molecular Microbiology 53 1343 1357

28. SmithTFWatermanMS 1981 Identification of Common Molecular Subsequences. Journal of Molecular Biology 147 195 197

29. OrtizARStraussCEMOlmeaO 2002 MAMMOTH (Matching molecular models obtained from theory): An automated method for model comparison. Protein Science 11 2606 2621

30. BassSGuQMChristenA 1996 Multicopy suppressors of prc mutant Escherichia coli include two HtrA (DegP) protease homologs (HhoAB), DksA, and a truncated RlpA. Journal of Bacteriology 178 1154 1161

31. BarbosaJARGSmithBJDeGoriROoiHCMarcuccioSM 2000 Active site modulation in the N-acetylneuraminate lyase sub-family as revealed by the structure of the inhibitor-complexed Haemophilus influenzae enzyme. Journal of Molecular Biology 303 405 421

32. JoergerACMayerSFershtAR 2003 Mimicking natural evolution in vitro: An N-acetylneuraminate lyase mutant with an increased dihydrodipicolinate synthase activity. Proceedings of the National Academy of Sciences of the United States of America 100 5694 5699

33. GauduPWeissB 2000 Flavodoxin mutants of Escherichia coli K-12. Journal of Bacteriology 182 1788 1793

34. AlbaBMLeedsJAOnufrykCLuCZGrossCA 2002 DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes & Development 16 2156 2168

35. DeLasPenasAConnollyLGrossCA 1997 The sigma(E)-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigma(E). Molecular Microbiology 24 373 385

36. YamanakaKOguraTKooninEVNikiHHiragaS 1994 Multicopy Suppressors, Mssa and Mssb, of an Smba Mutation of Escherichia-Coli. Molecular & General Genetics 243 9 16

37. XiaoHKalmanMIkeharaKZemelSGlaserG 1991 Residual Guanosine 3′,5′-Bispyrophosphate Synthetic Activity of Rela Null Mutants Can Be Eliminated by Spot Null Mutations. Journal of Biological Chemistry 266 5980 5990

38. CashelMGentryDRHernandezVJVinellaD 1996 The stringent response. NeidhardtFCIngrahamJLLinECCLowKBMagasanikB Escherichia coli and Salmonella: cellular and molecular biology. 2 ed Washington D.C. American Society of Microbiology

39. AshburnerMBallCABlakeJABotsteinDButlerH 2000 Gene Ontology: tool for the unification of biology. Nature Genetics 25 25 29

40. CampbellTLEdererCSAllali-HassaniABrownED 2007 Isolation of the rstA gene as a multicopy suppressor of YjeE, an essential ATPase of unknown function in Escherichia coli. Journal of Bacteriology 189 3318 3321

41. CampbellTLBrownED 2008 Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. Journal of Bacteriology 190 2537 2545

42. BlattnerFRPlunkettGBlochCAPernaNTBurlandV 1997 The complete genome sequence of Escherichia coli K-12. Science 277 1453 &

43. YuDGEllisHMLeeECJenkinsNACopelandNG 2000 An efficient recombination system for chromosome engineering in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 97 5978 5983

44. ChungCTNiemelaSLMillerRH 1989 One-Step Preparation of Competent Escherichia-Coli - Transformation and Storage of Bacterial-Cells in the Same Solution. Proceedings of the National Academy of Sciences of the United States of America 86 2172 2175

45. MillerJH 1972 Experiments in molecular genetics New York Cold Spring Harbor Laboratory Press

46. CherepanovPPWackernagelW 1995 Gene Disruption in Escherichia-Coli - Tcr and Km(R) Cassettes with the Option of Flp-Catalyzed Excision of the Antibiotic-Resistance Determinant. Gene 158 9 14

47. BergmillerTPena-MillerRBoehmAAckermannM 2011 Single-cell time-lapse analysis of depletion of the universally conserved essential protein YgjD. Bmc Microbiology 11

48. RouxABeloinCGhigoJM 2005 Combined inactivation and expression strategy to study gene function under physiological conditions: Application to identification of new Escherichia coli adhesins. Journal of Bacteriology 187 1001 1013

49. DatsenkoKAWannerBL 2000 One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proceedings of the National Academy of Sciences of the United States of America 97 6640 6645

50. KitagawaMAraTArifuzzamanMIoka-NakamichiTInamotoE 2005 Complete set of ORF clones of Escherichia coli ASKA library (A complete Set of E. coli K-12 ORF archive): Unique resources for biological research. DNA Research 12 291 299

51. BrickmanEBeckwithJ 1975 Analysis of Regulation of Escherichia-Coli Alkaline-Phosphatase Synthesis Using Deletions and Phi-80 Transducing Phages. Journal of Molecular Biology 96 307 316

52. WallDPFraserHBHirshAE 2003 Detecting putative orthologs. Bioinformatics 19 1710 1711

53. EdgarRC 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32 1792 1797

54. TalaveraGCastresanaJ 2007 Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56 564 577

55. RonquistFHuelsenbeckJP 2003 MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 1572 1574

56. R Development Core Team 2007 R: A Language and Environment for Statistical Computing

57. WeberHPesaventoCPosslingATischendorfGHenggeR 2006 Cyclic-di-GMP-mediated signalling within the sigma(S) network of Escherichia coli. Molecular Microbiology 62 1014 1034

58. DouchinVBohnCBoulocP 2006 Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. Journal of Biological Chemistry 281 12253 12259

59. CairraoFChoraAZilhaoRCarpousisAJArraianoCM 2001 RNase II levels change according to the growth conditions: characterization of gmr, a new Escherichia coli gene involved in the modulation of RNase II. Molecular Microbiology 39 1550 1561

60. BeggKJDewarSJDonachieWD 1995 A New Escherichia-Coli Cell-Division Gene, Ftsk. Journal of Bacteriology 177 6211 6222

61. KalamorzFReichenbachBMarzWRakBGorkeB 2007 Feedback control of glucosamine-6-phosphate synthase GlmS expression depends on the small RNA GlmZ and involves the novel protein YhbJ in Escherichia coli. Molecular Microbiology 65 1518 1533

62. DraperGCMcLennanNBeggKMastersMDonachieWD 1998 Only the N-terminal domain of FtsK functions in cell division. Journal of Bacteriology 180 4621 4627

63. WuTMcCandlishACGronenbergLSChngSSSilhavyTJ 2006 Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 103 11754 11759

64. MillerCThomsenLEGaggeroCMosseriRIngmerH 2004 SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 305 1629 1631

65. GuarinoEJimenez-SanchezAGuzmanEC 2007 Defective ribonucleoside diphosphate reductase impairs replication fork progression in Escherichia coli. Journal of Bacteriology 189 3496 3501

66. MileykovskayaESunQMargolinWDowhanW 1998 Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine. Journal of Bacteriology 180 4252 4257

67. RaetzCRHKantorGDNishijimaMNewmanKF 1979 Cardiolipin Accumulation in the Inner and Outer Membranes of Escherichia-Coli Mutants Defective in Phosphatidylserine Synthetase. Journal of Bacteriology 139 544 551

68. SrinivasanMMehtaPYuYPrugarEKooninEV 2011 The highly conserved KEOPS/EKC complex is essential for a universal tRNA modification, t6A. Embo Journal 30 873 881

69. RichardsonJP 1991 Preventing the Synthesis of Unused Transcripts by Rho-Factor. Cell 64 1047 1049

70. HashimotoCSakaguchiKTaniguchiYHondaHOshimaT 2011 Effects on Transcription of Mutations in ygjD, yeaZ, and yjeE Genes, Which Are Involved in a Universal tRNA Modification in Escherichia coli. Journal of Bacteriology 193 6075 6079

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