The segregation of bacterial chromosomes follows a precise choreography of spatial organisation. It is initiated by the bipolar migration of the sister copies of the replication origin (ori). Most bacterial chromosomes contain a partition system (Par) with parS sites in close proximity to ori that contribute to the active mobilisation of the ori region towards the old pole. This is thought to result in a longitudinal chromosomal arrangement within the cell. In this study, we followed the duplication frequency and the cellular position of 19 Vibrio cholerae genome loci as a function of cell length. The genome of V. cholerae is divided between two chromosomes, chromosome I and II, which both contain a Par system. The ori region of chromosome I (oriI) is tethered to the old pole, whereas the ori region of chromosome II is found at midcell. Nevertheless, we found that both chromosomes adopted a longitudinal organisation. Chromosome I extended over the entire cell while chromosome II extended over the younger cell half. We further demonstrate that displacing parS sites away from the oriI region rotates the bulk of chromosome I. The only exception was the region where replication terminates, which still localised to the septum. However, the longitudinal arrangement of chromosome I persisted in Par mutants and, as was reported earlier, the ori region still localised towards the old pole. Finally, we show that the Par-independent longitudinal organisation and oriI polarity were perturbed by the introduction of a second origin. Taken together, these results suggest that the Par system is the major contributor to the longitudinal organisation of chromosome I but that the replication program also influences the arrangement of bacterial chromosomes.
Vyšlo v časopise: The Two Cis-Acting Sites, and , Contribute to the Longitudinal Organisation of Chromosome I. PLoS Genet 10(7): e32767. doi:10.1371/journal.pgen.1004448 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004448
1. KuempelPL, HensonJM, DircksL, TecklenburgM, LimDF (1991) dif, a recA-independent recombination site in the terminus region of the chromosome of Escherichia coli. New Biol 3 : 799–811.
2. PossozC, JunierI, EspeliO (2012) Bacterial chromosome segregation. Front Biosci 17 : 1020–1034.
3. Vallet-GelyI, BoccardF (2013) Chromosomal organization and segregation in Pseudomonas aeruginosa. PLoS Genet 9: e1003492.
4. HarmsA, Treuner-LangeA, SchumacherD, Sogaard-AndersenL Tracking of Chromosome and Replisome Dynamics in Myxococcus xanthus Reveals a Novel Chromosome Arrangement. PLoS Genet 9: e1003802.
5. ViollierPH, ShapiroL (2004) Spatial complexity of mechanisms controlling a bacterial cell cycle. Curr Opin Microbiol 7 : 572–578.
6. SrivastavaP, FeketeRA, ChattorajDK (2006) Segregation of the replication terminus of the two Vibrio cholerae chromosomes. J Bacteriol 188 : 1060–1070.
7. FiebigA, KerenK, TheriotJA (2006) Fine-scale time-lapse analysis of the biphasic, dynamic behaviour of the two Vibrio cholerae chromosomes. Mol Microbiol 60 : 1164–1178.
8. FogelMA, WaldorMK (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev 20 : 3269–3282.
9. LivnyJ, YamaichiY, WaldorMK (2007) Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 189 : 8693–8703.
10. VecchiarelliAG, MizuuchiK, FunnellBE Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 86 : 513–523.
11. SaljeJ, GayathriP, LoweJ (2010) The ParMRC system: molecular mechanisms of plasmid segregation by actin-like filaments. Nat Rev Microbiol 8 : 683–692.
12. OguraT, HiragaS (1983) Partition mechanism of F plasmid: two plasmid gene-encoded products and a cis-acting region are involved in partition. Cell 32 : 351–360.
13. MartinKA, FriedmanSA, AustinSJ (1987) Partition site of the P1 plasmid. Proc Natl Acad Sci U S A 84 : 8544–8547.
14. ThanbichlerM, ShapiroL (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126 : 147–162.
15. YamaichiY, FogelMA, WaldorMK (2007) par genes and the pathology of chromosome loss in Vibrio cholerae. Proc Natl Acad Sci U S A 104 : 630–635.
16. LasockiK, BartosikAA, MierzejewskaJ, ThomasCM, Jagura-BurdzyG (2007) Deletion of the parA (soj) homologue in Pseudomonas aeruginosa causes ParB instability and affects growth rate, chromosome segregation, and motility. J Bacteriol 189 : 5762–5772.
17. IretonK, GuntherNWt, GrossmanAD (1994) spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176 : 5320–5329.
18. YamaichiY, FogelMA, McLeodSM, HuiMP, WaldorMK (2007) Distinct centromere-like parS sites on the two chromosomes of Vibrio spp. J Bacteriol 189 : 5314–5324.
19. MurrayH, ErringtonJ (2008) Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135 : 74–84.
20. KadoyaR, BaekJH, SarkerA, ChattorajDK (2011) Participation of chromosome segregation protein ParAI of Vibrio cholerae in chromosome replication. J Bacteriol 193 : 1504–1514.
21. GruberS, ErringtonJ (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137 : 685–696.
22. SullivanNL, MarquisKA, RudnerDZ (2009) Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137 : 697–707.
23. MinnenA, AttaiechL, ThonM, GruberS, VeeningJW (2011) SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae. Mol Microbiol 81 : 676–688.
24. PtacinJL, LeeSF, GarnerEC, ToroE, EckartM, et al. (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12 : 791–798.
25. SchofieldWB, LimHC, Jacobs-WagnerC (2010) Cell cycle coordination and regulation of bacterial chromosome segregation dynamics by polarly localized proteins. EMBO J 29 : 3068–3081.
26. ShebelutCW, GubermanJM, van TeeffelenS, YakhninaAA, GitaiZ (2010) Caulobacter chromosome segregation is an ordered multistep process. Proc Natl Acad Sci U S A 107 : 14194–14198.
27. YamaichiY, BrucknerR, RinggaardS, MollA, CameronDE, et al. (2012) A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev 26 : 2348–2360.
28. LalouxG, Jacobs-WagnerC (2013) Spatiotemporal control of PopZ localization through cell cycle-coupled multimerization. J Cell Biol 201 : 827–841.
29. ViollierPH, ThanbichlerM, McGrathPT, WestL, MeewanM, et al. (2004) Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Natl Acad Sci U S A 101 : 9257–9262.
30. UmbargerMA, ToroE, WrightMA, PorrecaGJ, BauD, et al. (2011) The three-dimensional architecture of a bacterial genome and its alteration by genetic perturbation. Mol Cell 44 : 252–264.
31. FogelMA, WaldorMK (2005) Distinct segregation dynamics of the two Vibrio cholerae chromosomes. Mol Microbiol 55 : 125–136.
32. KahngLS, ShapiroL (2003) Polar localization of replicon origins in the multipartite genomes of Agrobacterium tumefaciens and Sinorhizobium meliloti. J Bacteriol 185 : 3384–3391.
33. WangX, LiuX, PossozC, SherrattDJ (2006) The two Escherichia coli chromosome arms locate to separate cell halves. Genes Dev 20 : 1727–1731.
34. NielsenHJ, OttesenJR, YoungrenB, AustinSJ, HansenFG (2006) The Escherichia coli chromosome is organized with the left and right chromosome arms in separate cell halves. Mol Microbiol 62 : 331–338.
35. RasmussenT, JensenRB, SkovgaardO (2007) The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle. EMBO J 26 : 3124–3131.
36. JoshiMC, BourniquelA, FisherJ, HoBT, MagnanD, et al. (2011) Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc Natl Acad Sci U S A 108 : 2765–2770.
37. BrezellecP, HoebekeM, HietMS, PasekS, FeratJL (2006) DomainSieve: a protein domain-based screen that led to the identification of dam-associated genes with potential link to DNA maintenance. Bioinformatics 22 : 1935–1941.
38. MercierR, PetitMA, SchbathS, RobinS, El KarouiM, et al. (2008) The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135 : 475–485.
39. DemarreG, GalliE, MuresanL, PalyE, DavidA, et al. (2014) Differential management of the replication terminus regions of the two Vibrio cholerae chromosomes during cell division. PLoS Genet [In Press].
40. WangX, LesterlinC, Reyes-LamotheR, BallG, SherrattDJ (2011) Replication and segregation of an Escherichia coli chromosome with two replication origins. Proc Natl Acad Sci U S A 108: E243–250.
41. ToroE, HongSH, McAdamsHH, ShapiroL (2008) Caulobacter requires a dedicated mechanism to initiate chromosome segregation. Proc Natl Acad Sci U S A 105 : 15435–15440.
42. BerkmenMB, GrossmanAD (2007) Subcellular positioning of the origin region of the Bacillus subtilis chromosome is independent of sequences within oriC, the site of replication initiation, and the replication initiator DnaA. Mol Microbiol 63 : 150–165.
43. DanilovaO, Reyes-LamotheR, PinskayaM, SherrattD, PossozC (2007) MukB colocalizes with the oriC region and is required for organization of the two Escherichia coli chromosome arms into separate cell halves. Mol Microbiol 65 : 1485–1492.
44. BadrinarayananA, LesterlinC, Reyes-LamotheR, SherrattD (2012) The Escherichia coli SMC complex, MukBEF, shapes nucleoid organization independently of DNA replication. J Bacteriol 194 : 4669–4676.
45. MarvigRL, BlokeschM Natural transformation of Vibrio cholerae as a tool–optimizing the procedure. BMC Microbiol 10 : 155.
46. SliusarenkoO, HeinritzJ, EmonetT, Jacobs-WagnerC High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80 : 612–627.
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
