Genome Engineering in : A Feasible Approach to Address Biological Issues

English version České info

Although bacteria with multipartite genomes are prevalent, our knowledge of the mechanisms maintaining their genome is very limited, and much remains to be learned about the structural and functional interrelationships of multiple chromosomes. Owing to its bi-chromosomal genome architecture and its importance in public health, Vibrio cholerae, the causative agent of cholera, has become a preferred model to study bacteria with multipartite genomes. However, most in vivo studies in V. cholerae have been hampered by its genome architecture, as it is difficult to give phenotypes to a specific chromosome. This difficulty was surmounted using a unique and powerful strategy based on massive rearrangement of prokaryotic genomes. We developed a site-specific recombination-based engineering tool, which allows targeted, oriented, and reciprocal DNA exchanges. Using this genetic tool, we obtained a panel of V. cholerae mutants with various genome configurations: one with a single chromosome, one with two chromosomes of equal size, and one with both chromosomes controlled by identical origins. We used these synthetic strains to address several biological questions—the specific case of the essentiality of Dam methylation in V. cholerae and the general question concerning bacteria carrying circular chromosomes—by looking at the effect of chromosome size on topological issues. In this article, we show that Dam, RctB, and ParA2/ParB2 are strictly essential for chrII origin maintenance, and we formally demonstrate that the formation of chromosome dimers increases exponentially with chromosome size.

Vyšlo v časopise: Genome Engineering in : A Feasible Approach to Address Biological Issues. PLoS Genet 8(1): e32767. doi:10.1371/journal.pgen.1002472
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002472

Souhrn

Zdroje

1. SuwantoAKaplanS 1989 Physical and genetic mapping of the Rhodobacter sphaeroides 2.4.1 genome: presence of two unique circular chromosomes. J Bacteriol 171 5850 5859

2. CasjensS 1998 The diverse and dynamic structure of bacterial genomes. Annu Rev Genet 32 339 377

3. EganESFogelMAWaldorMK 2005 Divided genomes: negotiating the cell cycle in prokaryotes with multiple chromosomes. Mol Microbiol 56 1129 1138

4. HeidelbergJFEisenJANelsonWCClaytonRAGwinnML 2000 DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406 477 483

5. ReenFJAlmagro-MorenoSUsseryDBoydEF 2006 The genomic code: inferring Vibrionaceae niche specialization. Nat Rev Microbiol 4 697 704

6. DryseliusRKurokawaKIidaT 2007 Vibrionaceae, a versatile bacterial family with evolutionarily conserved variability. Res Microbiol 158 479 486

7. Le RouxFZouineMChakrounNBinesseJSaulnierD 2009 Genome sequence of Vibrio splendidus: an abundant planctonic marine species with a large genotypic diversity. Environ Microbiol 11 1959 1970

8. OkadaKIidaTKita-TsukamotoKHondaT 2005 Vibrios commonly possess two chromosomes. J Bacteriol 187 752 757

9. DemarreGChattorajDK 2010 DNA adenine methylation is required to replicate both Vibrio cholerae chromosomes once per cell cycle. PLoS Genet 6 e1000939 doi:10.1371/journal.pgen.1000939

10. DryseliusRIzutsuKHondaTIidaT 2008 Differential replication dynamics for large and small Vibrio chromosomes affect gene dosage, expression and location. BMC Genomics 9 559

11. DuigouSKnudsenKGSkovgaardOEganESLobner-OlesenA 2006 Independent control of replication initiation of the two Vibrio cholerae chromosomes by DnaA and RctB. J Bacteriol 188 6419 6424

12. EganESWaldorMK 2003 Distinct replication requirements for the two Vibrio cholerae chromosomes. Cell 114 521 530

13. FogelMAWaldorMK 2005 Distinct segregation dynamics of the two Vibrio cholerae chromosomes. Mol Microbiol 55 125 136

14. FogelMAWaldorMK 2006 A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20 3269 3282

15. PalDVenkova-CanovaTSrivastavaPChattorajDK 2005 Multipartite regulation of rctB, the replication initiator gene of Vibrio cholerae chromosome II. J Bacteriol 187 7167 7175

16. RasmussenTJensenRBSkovgaardO 2007 The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle. EMBO J 26 3124 3131

17. SrivastavaPChattorajDK 2007 Selective chromosome amplification in Vibrio cholerae. Mol Microbiol 66 1016 1028

18. SrivastavaPFeketeRAChattorajDK 2006 Segregation of the replication terminus of the two Vibrio cholerae chromosomes. J Bacteriol 188 1060 1070

19. ValMEKennedySPEl KarouiMBonneLChevalierF 2008 FtsK-dependent dimer resolution on multiple chromosomes in the pathogen Vibrio cholerae. PLoS Genet 4 e1000201 doi:10.1371/journal.pgen.1000201

20. YamaichiYFogelMAWaldorMK 2007 par genes and the pathology of chromosome loss in Vibrio cholerae. Proc Natl Acad Sci U S A 104 630 635

21. SchmidMFernandez-BadilloAFeichtingerWSteinleinCRomanJI 1988 On the highest chromosome number in mammals. Cytogenet Cell Genet 49 305 308

22. DuigouSYamaichiYWaldorMK 2008 ATP negatively regulates the initiator protein of Vibrio cholerae chromosome II replication. Proc Natl Acad Sci U S A 105 10577 10582

23. YamaichiYDuigouSShakhnovichEAWaldorMK 2009 Targeting the replication initiator of the second Vibrio chromosome: towards generation of vibrionaceae-specific antimicrobial agents. PLoS Pathog 5 e1000663 doi:10.1371/journal.ppat.1000663

24. EganESLobner-OlesenAWaldorMK 2004 Synchronous replication initiation of the two Vibrio cholerae chromosomes. Curr Biol 14 R501 502

25. Lobner-OlesenASkovgaardOMarinusMG 2005 Dam methylation: coordinating cellular processes. Curr Opin Microbiol 8 154 160

26. JulioSMHeithoffDMProvenzanoDKloseKESinsheimerRL 2001 DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae. Infect Immun 69 7610 7615

27. KahngLSShapiroL 2001 The CcrM DNA methyltransferase of Agrobacterium tumefaciens is essential, and its activity is cell cycle regulated. J Bacteriol 183 3065 3075

28. RobertsonGTReisenauerAWrightRJensenRBJensenA 2000 The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182 3482 3489

29. WrightRStephensCShapiroL 1997 The CcrM DNA methyltransferase is widespread in the alpha subdivision of proteobacteria, and its essential functions are conserved in Rhizobium meliloti and Caulobacter crescentus. J Bacteriol 179 5869 5877

30. KochBMaXLobner-OlesenA 2010 Replication of Vibrio cholerae chromosome I in Escherichia coli: dependence on dam methylation. J Bacteriol 192 3903 3914

31. DraperGCGoberJW 2002 Bacterial chromosome segregation. Annu Rev Microbiol 56 567 597

32. LeonardTAMoller-JensenJLoweJ 2005 Towards understanding the molecular basis of bacterial DNA segregation. Philos Trans R Soc Lond B Biol Sci 360 523 535

33. LesterlinCBarreFXCornetF 2004 Genetic recombination and the cell cycle: what we have learned from chromosome dimers. Mol Microbiol 54 1151 1160

34. CampoNDiasMJDaveran-MingotMLRitzenthalerPLe BourgeoisP 2004 Chromosomal constraints in Gram-positive bacteria revealed by artificial inversions. Mol Microbiol 51 511 522

35. EsnaultEValensMEspeliOBoccardF 2007 Chromosome structuring limits genome plasticity in Escherichia coli. PLoS Genet 3 e226 doi:10.1371/journal.pgen.0030226

36. GuijoMIPatteJdel Mar CamposMLouarnJMRebolloJE 2001 Localized remodeling of the Escherichia coli chromosome: the patchwork of segments refractory and tolerant to inversion near the replication terminus. Genetics 157 1413 1423

37. HillCWGrayJA 1988 Effects of chromosomal inversion on cell fitness in Escherichia coli K-12. Genetics 119 771 778

38. LesterlinCMercierRBoccardFBarreFXCornetF 2005 Roles for replichores and macrodomains in segregation of the Escherichia coli chromosome. EMBO Rep 6 557 562

39. LiuGRLiuWQJohnstonRNSandersonKELiSX 2006 Genome plasticity and ori-ter rebalancing in Salmonella typhi. Mol Biol Evol 23 365 371

40. LouarnJMBoucheJPLegendreFLouarnJPatteJ 1985 Characterization and properties of very large inversions of the E. coli chromosome along the origin-to-terminus axis. Mol Gen Genet 201 467 476

41. MieselLSegallARothJR 1994 Construction of chromosomal rearrangements in Salmonella by transduction: inversions of non-permissive segments are not lethal. Genetics 137 919 932

42. RebolloJEFrancoisVLouarnJM 1988 Detection and possible role of two large nondivisible zones on the Escherichia coli chromosome. Proc Natl Acad Sci U S A 85 9391 9395

43. RochaEPDanchinA 2003 Gene essentiality determines chromosome organisation in bacteria. Nucleic Acids Res 31 6570 6577

44. SegallAMahanMJRothJR 1988 Rearrangement of the bacterial chromosome: forbidden inversions. Science 241 1314 1318

45. CuiTMoro-okaNOhsumiKKodamaKOhshimaT 2007 Escherichia coli with a linear genome. EMBO Rep 8 181 187

46. ItayaMTanakaT 1997 Experimental surgery to create subgenomes of Bacillus subtilis 168. Proc Natl Acad Sci U S A 94 5378 5382

47. KolisnychenkoVPlunkettG3rdHerringCDFeherTPosfaiJ 2002 Engineering a reduced Escherichia coli genome. Genome Res 12 640 647

48. VolffJNViellPAltenbuchnerJ 1997 Artificial circularization of the chromosome with concomitant deletion of its terminal inverted repeats enhances genetic instability and genome rearrangement in Streptomyces lividans. Mol Gen Genet 253 753 760

49. HendricksonHLawrenceJG 2006 Selection for chromosome architecture in bacteria. J Mol Evol 62 615 629

50. LouarnJMKuempelPCornetF 2005 The terminus region of the E. coli chromosome, or, all's well that ends well. HigginsNP The Bacterial Chromosome Washington, D.C. ASM press 251 273

51. RochaEP 2008 The organization of the bacterial genome. Annu Rev Genet 42 211 233

52. VesthTWassenaarTMHallinPFSnipenLLagesenK 2010 On the origins of a Vibrio species. Microb Ecol 59 1 13

53. WeisbergRAGottesmannMEHendrixRWLittleJW 1999 Family values in the age of genomics: comparative analyses of temperate bacteriophage HK022. Annu Rev Genet 33 565 602

54. SauerB 1996 Multiplex Cre/lox recombination permits selective site-specific DNA targeting to both a natural and an engineered site in the yeast genome. Nucleic Acids Res 24 4608 4613

55. TuranSKuehleJSchambachABaumCBodeJ 2010 Multiplexing RMCE: versatile extensions of the Flp-recombinase-mediated cassette-exchange technology. J Mol Biol 402 52 69

56. GottesmanMEWeisbergRA 1971 Prophage Insertion and Excision. HersheyAD Lambda: Cold Spring Harbor Laboratory 113 138

57. YamaichiYFogelMAMcLeodSMHuiMPWaldorMK 2007 Distinct centromere-like parS sites on the two chromosomes of Vibrio spp. J Bacteriol 189 5314 5324

58. AustinSNordstromK 1990 Partition-mediated incompatibility of bacterial plasmids. Cell 60 351 354

59. MarinusMGCasadesusJ 2009 Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. FEMS Microbiol Rev 33 488 503

60. PeralsKCornetFMerletYDelonILouarnJM 2000 Functional polarization of the Escherichia coli chromosome terminus: the dif site acts in chromosome dimer resolution only when located between long stretches of opposite polarity. Mol Microbiol 36 33 43

61. SteinerWWKuempelPL 1998 Sister chromatid exchange frequencies in Escherichia coli analyzed by recombination at the dif resolvase site. J Bacteriol 180 6269 6275

62. CoxMMGoodmanMFKreuzerKNSherrattDJSandlerSJ 2000 The importance of repairing stalled replication forks. Nature 404 37 41

63. CromieGALeachDR 2000 Control of crossing over. Mol Cell 6 815 826

64. MichelBRecchiaGDPenel-ColinMEhrlichSDSherrattDJ 2000 Resolution of holliday junctions by RuvABC prevents dimer formation in rep mutants and UV-irradiated cells. Mol Microbiol 37 180 191

65. CouturierERochaEP 2006 Replication-associated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Mol Microbiol 59 1506 1518

66. CambrayGMutalikVKArkinAP 2011 Toward rational design of bacterial genomes. Curr Opin Microbiol

67. GibsonDGBendersGAAndrews-PfannkochCDenisovaEABaden-TillsonH 2008 Complete chemical synthesis, assembly, and cloning of a Mycoplasma genitalium genome. Science 319 1215 1220

68. LartigueCVasheeSAlgireMAChuangRYBendersGA 2009 Creating bacterial strains from genomes that have been cloned and engineered in yeast. Science 325 1693 1696

69. CarrPAChurchGM 2009 Genome engineering. Nat Biotechnol 27 1151 1162

70. GuoXFloresMMavinguiPFuentesSIHernandezG 2003 Natural genomic design in Sinorhizobium meliloti: novel genomic architectures. Genome Res 13 1810 1817

71. Le RouxFBinesseJSaulnierDMazelD 2007 Construction of a Vibrio splendidus mutant lacking the metalloprotease gene vsm by use of a novel counterselectable suicide vector. Appl Environ Microbiol 73 777 784

72. GuerinECambrayGSanchez-AlberolaNCampoySErillI 2009 The SOS response controls integron recombination. Science 324 1034

73. CherepanovPPWackernagelW 1995 Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158 9 14

74. 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

75. IidaTSuthienkulOParkKSTangGQYamamotoRK 1997 Evidence for genetic linkage between the ure and trh genes in Vibrio parahaemolyticus. J Med Microbiol 46 639 645

76. CooperSHelmstetterCE 1968 Chromosome replication and the division cycle of Escherichia coli B/r. J Mol Biol 31 519 540

77. MichelsenOTeixeira de MattosMJJensenPRHansenFG 2003 Precise determinations of C and D periods by flow cytometry in Escherichia coli K-12 and B/r. Microbiology 149 1001 1010

78. SkarstadKSteenHBBoyeE 1985 Escherichia coli DNA distributions measured by flow cytometry and compared with theoretical computer simulations. J Bacteriol 163 661 668