1887

Microbiology Society logo

Volume 165, Issue 12

origin of chromosomal replication with two putative unwinding elements Free

Abstract

DNA replication is controlled mostly at the initiation step. In bacteria, replication of the chromosome starts at a single origin of replication called . The initiator protein, DnaA, binds to specific sequences (DnaA boxes) within and assembles into a filament that promotes DNA double helix opening within the DNA unwinding element (DUE). This process has been thoroughly examined in model bacteria, including and but we have a relatively limited understanding of chromosomal replication initiation in other species. Here, we reveal new details of DNA replication initiation in , a group of Gram-positive soil bacteria that possesses a long linear (8–10 Mbps) and GC-rich chromosome with a centrally positioned . We used comprehensive and analyses to better characterize the structure of . We identified 14 DnaA-binding motifs and determined the consensus sequence of the DnaA box. Unexpectedly, our analysis using the WebSIDD algorithm revealed the presence of two putative DUEs (DUE1 and DUE2) located very near one another toward the 5′ end of the region. P1 nuclease assay revealed that DNA unwinding occurs at both of the proposed sites, but using an replication initiation point mapping we were able to confirm only one of them (DUE2). The previously observed transcriptional activity of the region may help explain the current results. We speculate that transcription itself could modulate activity in by determining whether DNA unwinding occurs at DUE1 or DUE2.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): DNA replication , oriC and Streptomyces
© 2019 The Authors
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000859
2019-12-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/165/12/1365.html?itemId=/content/journal/micro/10.1099/mic.0.000859&mimeType=html&fmt=ahah

References

  1. Boye E, Løbner-Olesen A, Skarstad K. Limiting DNA replication to once and only once. EMBO Rep 2000; 1:479–483 [View Article]
     [Google Scholar]
  2. Leonard AC, Grimwade JE. Regulating DnaA complex assembly: it is time to fill the gaps. Curr Opin Microbiol 2010; 13:766–772 [View Article]
     [Google Scholar]
  3. Ozaki S, Katayama T. Dnaa structure, function, and dynamics in the initiation at the chromosomal origin. Plasmid 2009; 62:71–82 [View Article]
     [Google Scholar]
  4. Wolański M, Donczew R, Zawilak-Pawlik A, Zakrzewska-Czerwińska J. oriC-encoded Instructions for the initiation of bacterial chromosome replication. Front Microbiol 2014; 5:735 [View Article]
     [Google Scholar]
  5. Hottes AK, Shapiro L, McAdams HH. Dnaa coordinates replication initiation and cell cycle transcription in Caulobacter crescentus . Mol Microbiol 2005; 58:1340–1353 [View Article]
     [Google Scholar]
  6. Jensen RB, Wang SC, Shapiro L. A moving DNA replication factory in Caulobacter crescentus . EMBO J 2001; 20:4952–4963 [View Article]
     [Google Scholar]
  7. Marczynski GT, Shapiro L. Cell-Cycle control of a cloned chromosomal origin of replication from Caulobacter crescentus . J Mol Biol 1992; 226:959–977 [View Article]
     [Google Scholar]
  8. Krause M, Rückert B, Lurz R, Messer W. Complexes at the replication origin of Bacillus subtilis with homologous and heterologous DnaA protein. J Mol Biol 1997; 274:365–380 [View Article]
     [Google Scholar]
  9. Richardson TT, Harran O, Murray H. The bacterial DnaA-trio replication origin element specifies single-stranded DNA initiator binding. Nature 2016; 534:412–416 [View Article]
     [Google Scholar]
  10. Roth A, Urmoneit B, Messer W. Functions of histone-like proteins in the initiation of DNA replication at oriC of Escherichia coli . Biochimie 1994; 76:917–923 [View Article]
     [Google Scholar]
  11. Ryan VT, Grimwade JE, Camara JE, Crooke E, Leonard AC. Escherichia coli prereplication complex assembly is regulated by dynamic interplay among FIS, IHF and DnaA. Mol Microbiol 2004; 51:1347–1359 [View Article]
     [Google Scholar]
  12. Katayama T, Ozaki S, Keyamura K, Fujimitsu K. Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC . Nat Rev Microbiol 2010; 8:163–170 [View Article]
     [Google Scholar]
  13. Donczew R, Zakrzewska-Czerwińska J, Zawilak-Pawlik A. Beyond DnaA: the role of DNA topology and DNA methylation in bacterial replication initiation. J Mol Biol 2014; 426:2269–2282 [View Article]
     [Google Scholar]
  14. Kasho K, Tanaka H, Sakai R, Katayama T. Cooperative DnaA Binding to the Negatively Supercoiled datA Locus Stimulates DnaA-ATP Hydrolysis. J Biol Chem 2017; 292:1251–1266 [View Article]
     [Google Scholar]
  15. Moriya S, Atlung T, Hansen FG, Yoshikawa H, Ogasawara N. Cloning of an autonomously replicating sequence (ARS) from the Bacillus subtilis chromosome. Mol Microbiol 1992; 6:309–315
     [Google Scholar]
  16. Donczew R, Weigel C, Lurz R, Zakrzewska-Czerwińska J, Zawilak-Pawlik A. Helicobacter pylori oriC--the first bipartite origin of chromosome replication in Gram-negative bacteria. Nucleic Acids Res 2012; 40:9647–9660 [View Article]
     [Google Scholar]
  17. Yee TW, Smith DW. Pseudomonas chromosomal replication origins: a bacterial class distinct from Escherichia coli-type origins. Proc Natl Acad Sci USA 1990; 87:1278–1282 [View Article]
     [Google Scholar]
  18. Jakimowicz D, Majka J, Messer W, Speck C, Fernandez M et al. Structural elements of the Streptomyces oriC region and their interactions with the DnaA protein. Microbiology 1998; 144:1281–1290 [View Article]
     [Google Scholar]
  19. Ruban-Ośmiałowska B, Jakimowicz D, Smulczyk-Krawczyszyn A, Chater KF, Zakrzewska-Czerwińska J. Replisome localization in vegetative and aerial hyphae of Streptomyces coelicolor . J Bacteriol 2006; 188:7311–7316 [View Article]
     [Google Scholar]
  20. Wolański M, Jakimowicz D, Zakrzewska-Czerwińska J. Adpa, key regulator for morphological differentiation regulates bacterial chromosome replication. Open Biol 2012; 2:120097 [View Article]
     [Google Scholar]
  21. Bentley SD, Chater KF, Cerdeño-Tárraga AM, Challis GL, Thomson NR et al. Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 2002; 417:141147 [View Article]
     [Google Scholar]
  22. Jakimowicz D, Majkadagger J, Konopa G, Wȩgrzyn G, Messer W et al. Architecture of the Streptomyces lividans DnaA protein-replication origin complexes. J Mol Biol 2000; 298:351–364 [View Article]
     [Google Scholar]
  23. Sambrook J, Fritsch EF, Maniatis T. “Molecular Cloning: A Laboratory Manual.”. Molecular Cloning: A Laboratory Manual 2 1989
     [Google Scholar]
  24. Stuttard C. Temperate phages of Streptomyces venezuelae: lysogeny and host specificity shown by phages SV1 and SV2. Microbiology 1982; 128:115–121 [View Article]
     [Google Scholar]
  25. Zhabinskaya D, Madden S, Benham CJ. SIST: stress-induced structural transitions in superhelical DNA. Bioinformatics 2015; 31:421–422 [View Article]
     [Google Scholar]
  26. Bi C, Benham CJ. WebSIDD: server for predicting stress-induced duplex destabilized (SIDD) sites in superhelical DNA. Bioinformatics 2004; 20:1477–1479 [View Article]
     [Google Scholar]
  27. Gust B, Chandra G, Jakimowicz D, Yuqing T, Bruton CJ et al. Lambda red-mediated genetic manipulation of antibiotic-producing Streptomyces . Adv Appl Microbiol 2004; 54:107–128 [View Article]
     [Google Scholar]
  28. Bibb MJ, Domonkos A, Chandra G, Buttner MJ. Expression of the chaplin and rodlin hydrophobic sheath proteins in Streptomyces venezuelae is controlled by σ(BldN) and a cognate anti-sigma factor, RsbN. Mol Microbiol 2012; 84:1033–1049 [View Article]
     [Google Scholar]
  29. Donczew M, Mackiewicz P, Wróbel A, Flärdh K, Zakrzewska-Czerwińska J et al. ParA and ParB coordinate chromosome segregation with cell elongation and division during Streptomyces sporulation. Open Biol 2016; 6:150263 [View Article]
     [Google Scholar]
  30. Patel MJ, Bhatia L, Yilmaz G, Biswas-Fiss EE, Biswas SB. Multiple conformational states of DnaA protein regulate its interaction with DnaA boxes in the initiation of DNA replication. Biochim Biophys Acta Gen Subj 2017; 1861:2165–2174 [View Article]
     [Google Scholar]
  31. Zawilak-Pawlik AM, Kois A, Zakrzewska-Czerwinska J. A simplified method for purification of recombinant soluble DnaA proteins. Protein Expr Purif 2006; 48:126–133 [View Article]
     [Google Scholar]
  32. Sasse-Dwight S, Gralla JD. Footprinting protein-DNA complexes in vivo. Methods Enzymol 1991; 208:146–148
     [Google Scholar]
  33. Cassler MR, Grimwade JE, Leonard AC. Cell cycle-specific changes in nucleoprotein complexes at a chromosomal replication origin. Embo J 1995; 14:5833–5841
     [Google Scholar]
  34. Gerbi SA, Bielinsky AK. Replication initiation point mapping. Methods 1997; 13:271–280 [View Article]
     [Google Scholar]
  35. Fujikawa N, Kurumizaka H, Nureki O, Terada T, Shirouzu M et al. Structural basis of replication origin recognition by the DnaA protein. Nucleic Acids Res 2003; 31:2077–2086 [View Article]
     [Google Scholar]
  36. Mott ML, Berger JM. Dna replication initiation: mechanisms and regulation in bacteria. Nat Rev Microbiol 2007; 5:343–354 [View Article]
     [Google Scholar]
  37. Ozaki S, Noguchi Y, Hayashi Y, Miyazaki E, Katayama T. Differentiation of the DnaA-oriC subcomplex for DNA unwinding in a replication initiation complex. J Biol Chem 2012; 287:37458–37471 [View Article]
     [Google Scholar]
  38. Katayama T, Kasho K, Kawakami H. The DnaA cycle in Escherichia coli: activation, function and inactivation of the initiator protein. Front Microbiol 2017; 8: [View Article]
     [Google Scholar]
  39. Majka J, Zakrzewska-Czerwiñska J, Messer W. Sequence recognition, cooperative interaction, and dimerization of the initiator protein DnaA of Streptomyces . J Biol Chem 2001; 276:6243–6252 [View Article]
     [Google Scholar]
  40. Majka J, Jakimowicz D, Messer W, Schrempf H, Lisowski M et al. Interactions of the Streptomyces lividans initiator protein DnaA with its target. Eur J Biochem 1999; 260:325–335 [View Article]
     [Google Scholar]
  41. Carey MF, Peterson CL, Smale ST. Dnase I footprinting. Cold Spring Harb Protoc 2013; 2013:469–478 [View Article]
     [Google Scholar]
  42. Majka J, Messer W, Schrempf H, Zakrzewska-Czerwińska J. Purification and characterization of the Streptomyces lividans initiator protein DnaA. J Bacteriol 1997; 179:2426–2432 [View Article]
     [Google Scholar]
  43. Zawilak-Pawlik A, Kois A, Majka J, Jakimowicz D, Smulczyk-Krawczyszyn A et al. Architecture of bacterial replication initiation complexes: orisomes from four unrelated bacteria. Biochem J 2005; 389:471–481 [View Article]
     [Google Scholar]
  44. Crooks GE, Hon G, Chandonia JM, Brenner SE. Weblogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article]
     [Google Scholar]
  45. Jaworski P, Donczew R, Mielke T, Thiel M, Oldziej S et al. Unique and universal features of epsilonproteobacterial origins of chromosome replication and DnaA-DnaA box interactions. Front Microbiol 2016; 7:1555 [View Article]
     [Google Scholar]
  46. Makowski Łukasz, Donczew R, Weigel C, Zawilak-Pawlik A, Zakrzewska-Czerwińska J. Initiation of chromosomal replication in predatory bacterium Bdellovibrio bacteriovorus . Front Microbiol 2016; 7: [View Article]
     [Google Scholar]
  47. Jaworski P, Donczew R, Mielke T, Weigel C, Stingl K et al. Structure and function of the Campylobacter jejuni chromosome replication origin. Front Microbiol 2018; 9:1533 [View Article]
     [Google Scholar]
  48. Richardson TT, Stevens D, Pelliciari S, Harran O, Sperlea T et al. Identification of a basal system for unwinding a bacterial chromosome origin. Embo J 2019; 38:e101649 [View Article]
     [Google Scholar]
  49. Hwang DS, Kornberg A. Opening of the replication origin of Escherichia coli by DnaA protein with protein HU or IHF. J Biol Chem 1992; 267:23083–23086
     [Google Scholar]
  50. Natrajan G, Noirot-Gros MF, Zawilak-Pawlik A, Kapp U, Terradot L. The structure of a DnaA/HobA complex from Helicobacter pylori provides insight into regulation of DNA replication in bacteria. Proc Natl Acad Sci USA 2009; 106:21115–21120 [View Article]
     [Google Scholar]
  51. Grimwade JE, Rozgaja TA, Gupta R, Dyson K, Rao P et al. Origin recognition is the predominant role for DnaA-ATP in initiation of chromosome replication. Nucleic Acids Res 2018; 46:6140–6151 [View Article]
     [Google Scholar]
  52. Das-Bradoo S, Bielinsky AK. Replication initiation point mapping: approach and implications. Methods Mol Biol 2009; 521:105–120 [View Article]
     [Google Scholar]
  53. Glazebrook MA, Doull JL, Stuttard C, Vining LC. Sporulation of Streptomyces venezuelae in submerged cultures. Microbiology 1990; 136:581–588
     [Google Scholar]
  54. Lee LF, Yeh SH, Chen CW. Construction and synchronization of dnaA temperature-sensitive mutants of Streptomyces . J Bacteriol 2002; 184:1214–1218 [View Article]
     [Google Scholar]
  55. Bird RE, Chandler M, Caro L. Suppression of an Escherichia coli dnaA mutation by the integrated R factor R.100.1: change of chromosome replication origin in synchronized cultures. J Bacteriol 1976; 126:1215–1223
     [Google Scholar]
  56. Zakrzewska-Czerwińska J, Majka J, Schrempf H. Minimal requirements of the Streptomyces lividans 66 oriC region and its transcriptional and translational activities. J Bacteriol 1995; 177:4765–4771 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000859
Loading
Streptomycete origin of chromosomal replication with two putative unwinding elements
Microbiology 165, 1365 (2019); https://doi.org/10.1099/mic.0.000859
/content/journal/micro/10.1099/mic.0.000859
/content/journal/micro/10.1099/mic.0.000859
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error