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Identification of a Single Strand Origin of Replication in the Integrative and Conjugative Element ICE of


Mobile genetic elements facilitate movement of genes, including those conferring antibiotic resistance and other traits, between bacteria. Integrative and conjugative elements (ICEs) are a large family of mobile genetic elements that are typically found integrated in the chromosome of their host bacterium. Under certain conditions (e.g., DNA damage, high cell density, stationary phase) an ICE excises from the host chromosome to form a circle. A linear single strand of ICE DNA can be transferred to an appropriate recipient through the ICE-encoded conjugation machinery. In addition, following excision from the chromosome, at least some (perhaps most) ICEs undergo autonomous rolling circle replication, a mechanism used by many plasmids and phages. Rolling circle replication generates single-stranded DNA (ssDNA). We found that ICEBs1, from Bacillus subtilis, contains at least two regions that enable conversion of ssDNA to double-stranded DNA. At least one of these regions functions as an sso (single strand origin of replication). ICEBs1 Sso activity was important for the ability of transferred ICEBs1 to be acquired by recipients and for the ability of ICEBs1 to replicate autonomously after excising from its host’s chromosome. We identified putative sso's in several other ICEs, indicating that Sso activity is likely important for the replication, stability and spread of these elements.


Vyšlo v časopise: Identification of a Single Strand Origin of Replication in the Integrative and Conjugative Element ICE of. PLoS Genet 11(10): e32767. doi:10.1371/journal.pgen.1005556
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005556

Souhrn

Mobile genetic elements facilitate movement of genes, including those conferring antibiotic resistance and other traits, between bacteria. Integrative and conjugative elements (ICEs) are a large family of mobile genetic elements that are typically found integrated in the chromosome of their host bacterium. Under certain conditions (e.g., DNA damage, high cell density, stationary phase) an ICE excises from the host chromosome to form a circle. A linear single strand of ICE DNA can be transferred to an appropriate recipient through the ICE-encoded conjugation machinery. In addition, following excision from the chromosome, at least some (perhaps most) ICEs undergo autonomous rolling circle replication, a mechanism used by many plasmids and phages. Rolling circle replication generates single-stranded DNA (ssDNA). We found that ICEBs1, from Bacillus subtilis, contains at least two regions that enable conversion of ssDNA to double-stranded DNA. At least one of these regions functions as an sso (single strand origin of replication). ICEBs1 Sso activity was important for the ability of transferred ICEBs1 to be acquired by recipients and for the ability of ICEBs1 to replicate autonomously after excising from its host’s chromosome. We identified putative sso's in several other ICEs, indicating that Sso activity is likely important for the replication, stability and spread of these elements.


Zdroje

1. Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3: 722–732. 16138100

2. Guglielmini J, Quintais L, Garcillan-Barcia MP, de la Cruz F, Rocha EP (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7: e1002222. doi: 10.1371/journal.pgen.1002222 21876676

3. Wilkins B, Lanka E (1993) DNA Processing and Replication during Plasmid Transfer between Gram-Negative Bacteria. In: Clewell DB, editor. Bacterial Conjugation: Springer US. pp. 105–136.

4. Alvarez-Martinez CE, Christie PJ (2009) Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73: 775–808. doi: 10.1128/MMBR.00023-09 19946141

5. Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD (2005) Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci U S A 102: 12554–12559. 16105942

6. Lee CA, Auchtung JM, Monson RE, Grossman AD (2007) Identification and characterization of int (integrase), xis (excisionase) and chromosomal attachment sites of the integrative and conjugative element ICEBs1 of Bacillus subtilis. Mol Microbiol 66: 1356–1369. 18005101

7. Lee CA, Grossman AD (2007) Identification of the origin of transfer (oriT) and DNA relaxase required for conjugation of the integrative and conjugative element ICEBs1 of Bacillus subtilis. J Bacteriol 189: 7254–7261. 17693500

8. Thomas J, Lee CA, Grossman AD (2013) A conserved helicase processivity factor is needed for conjugation and replication of an integrative and conjugative element. PLoS Genet 9: e103198.

9. Berkmen MB, Lee CA, Loveday EK, Grossman AD (2010) Polar positioning of a conjugation protein from the integrative and conjugative element ICEBs1 of Bacillus subtilis. J Bacteriol 192: 38–45. doi: 10.1128/JB.00860-09 19734305

10. DeWitt T, Grossman AD (2014) The bifunctional cell wall hydrolase CwlT is needed for conjugation of the integrative and conjugative element ICEBs1 in Bacillus subtilis and B. anthracis. J Bacteriol 196: 1588–1596. doi: 10.1128/JB.00012-14 24532767

11. Burrus V, Pavlovic G, Decaris B, Guedon G (2002) The ICESt1 element of Streptococcus thermophilus belongs to a large family of integrative and conjugative elements that exchange modules and change their specificity of integration. Plasmid 48: 77–97. 12383726

12. Auchtung JM, Lee CA, Garrison KL, Grossman AD (2007) Identification and characterization of the immunity repressor (ImmR) that controls the mobile genetic element ICEBs1 of Bacillus subtilis. Mol Microbiol 64: 1515–1528. 17511812

13. Bose B, Auchtung JM, Lee CA, Grossman AD (2008) A conserved anti-repressor controls horizontal gene transfer by proteolysis. Mol Microbiol 70: 570–582. doi: 10.1111/j.1365-2958.2008.06414.x 18761623

14. Lawley TD, Klimke WA, Gubbins MJ, Frost LS (2003) F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 224: 1–15. 12855161

15. Ohki M, Tomizawa J (1968) Asymmetric transfer of DNA strands in bacterial conjugation. Cold Spring Harb Symp Quant Biol 33: 651–658. 4892002

16. Yusibov VM, Steck TR, Gupta V, Gelvin SB (1994) Association of single-stranded transferred DNA from Agrobacterium tumefaciens with tobacco cells. Proc Natl Acad Sci U S A 91: 2994–2998. 8159693

17. Tinland B, Hohn B, Puchta H (1994) Agrobacterium tumefaciens transfers single-stranded transferred DNA (T-DNA) into the plant cell nucleus. Proc Natl Acad Sci U S A 91: 8000–8004. 11607492

18. Willetts N, Wilkins B (1984) Processing of plasmid DNA during bacterial conjugation. Microbiol Rev 48: 24–41. 6201705

19. Draper O, Cesar CE, Machon C, de la Cruz F, Llosa M (2005) Site-specific recombinase and integrase activities of a conjugative relaxase in recipient cells. Proc Natl Acad Sci U S A 102: 16385–16390. 16260740

20. Lanka E, Wilkins BM (1995) DNA processing reactions in bacterial conjugation. Annu Rev Biochem 64: 141–169. 7574478

21. Chandler M, de la Cruz F, Dyda F, Hickman AB, Moncalian G, et al. (2013) Breaking and joining single-stranded DNA: the HUH endonuclease superfamily. Nat Rev Microbiol 11: 525–538. doi: 10.1038/nrmicro3067 23832240

22. Rajeev L, Malanowska K, Gardner JF (2009) Challenging a paradigm: the role of DNA homology in tyrosine recombinase reactions. Microbiol Mol Biol Rev 73: 300–309. doi: 10.1128/MMBR.00038-08 19487729

23. Khan SA (2005) Plasmid rolling-circle replication: highlights of two decades of research. Plasmid 53: 126–136. 15737400

24. Khan SA (1997) Rolling-circle replication of bacterial plasmids. Microbiol Mol Biol Rev 61: 442–455. 9409148

25. Masai H, Arai K (1996) Mechanisms of primer RNA synthesis and D-loop/R-loop-dependent DNA replication in Escherichia coli. Biochimie 78: 1109–1117. 9150892

26. Meijer WJ, van der Lelie D, Venema G, Bron S (1995) Effects of the generation of single-stranded DNA on the maintenance of plasmid pMV158 and derivatives in different Bacillus subtilis strains. Plasmid 33: 79–89. 7597110

27. Seegers JF, Zhao AC, Meijer WJ, Khan SA, Venema G, et al. (1995) Structural and functional analysis of the single-strand origin of replication from the lactococcal plasmid pWV01. Mol Gen Genet 249: 43–50. 8552032

28. Lorenzo-Diaz F, Espinosa M (2009) Lagging-strand DNA replication origins are required for conjugal transfer of the promiscuous plasmid pMV158. J Bacteriol 191: 720–727. doi: 10.1128/JB.01257-08 19028894

29. Gruss AD, Ross HF, Novick RP (1987) Functional analysis of a palindromic sequence required for normal replication of several staphylococcal plasmids. Proc Natl Acad Sci U S A 84: 2165–2169. 3104910

30. Lee CA, Babic A, Grossman AD (2010) Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol 75: 268–279. doi: 10.1111/j.1365-2958.2009.06985.x 19943900

31. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402. 9254694

32. Uozumi T, Ozaki A, Beppu T, Arima K (1980) New cryptic plasmid of Bacillus subtilis and restriction analysis of other plasmids found by general screening. J Bacteriol 142: 315–318. 6246066

33. Meijer WJ, Wisman GB, Terpstra P, Thorsted PB, Thomas CM, et al. (1998) Rolling-circle plasmids from Bacillus subtilis: complete nucleotide sequences and analyses of genes of pTA1015, pTA1040, pTA1050 and pTA1060, and comparisons with related plasmids from gram-positive bacteria. FEMS Microbiol Rev 21: 337–368. 9532747

34. Notredame C, Higgins DG, Heringa J (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205–217. 10964570

35. Seery L, Devine KM (1993) Analysis of features contributing to activity of the single-stranded origin of Bacillus plasmid pBAA1. J Bacteriol 175: 1988–1994. 8458841

36. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research 31: 3406–3415. 12824337

37. Haima P, Bron S, Venema G (1987) The effect of restriction on shotgun cloning and plasmid stability in Bacillus subtilis Marburg. Mol Gen Genet 209: 335–342. 2823077

38. Bruand C, Ehrlich SD, Janniere L (1995) Primosome assembly site in Bacillus subtilis. EMBO J 14: 2642–2650. 7781616

39. Bron S, Meijer W, Holsappel S, Haima P (1991) Plasmid instability and molecular cloning in Bacillus subtilis. Res Microbiol 142: 875–883. 1664537

40. Berkmen MB, Grossman AD (2006) Spatial and temporal organization of the Bacillus subtilis replication cycle. Mol Microbiol 62: 57–71. 16942601

41. Wagner JK, Marquis KA, Rudner DZ (2009) SirA enforces diploidy by inhibiting the replication initiator DnaA during spore formation in Bacillus subtilis. Mol Microbiol 73: 963–974. doi: 10.1111/j.1365-2958.2009.06825.x 19682252

42. Milne TA, Zhao K, Hess JL (2009) Chromatin immunoprecipitation (ChIP) for analysis of histone modifications and chromatin-associated proteins. Methods Mol Biol 538: 409–423. doi: 10.1007/978-1-59745-418-6_21 19277579

43. Menard KL, Grossman AD (2013) Selective pressures to maintain attachment site specificity of integrative and conjugative elements. PLoS Genet 9: e1003623. doi: 10.1371/journal.pgen.1003623 23874222

44. Val M-E, Bouvier M, Campos J, Sherratt D, Cornet Fß, et al. (2005) The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae. Molecular Cell 19: 559–566. 16109379

45. Bouvier M, Demarre G, Mazel D (2005) Integron cassette insertion: a recombination process involving a folded single strand substrate. EMBO J 24: 4356–4367. 16341091

46. Horinouchi S, Weisblum B (1982) Nucleotide sequence and functional map of pC194, a plasmid that specifies inducible chloramphenicol resistance. J Bacteriol 150: 815–825. 6950931

47. Khan SA, Novick RP (1983) Complete nucleotide sequence of pT181, a tetracycline-resistance plasmid from Staphylococcus aureus. Plasmid 10: 251–259. 6657777

48. McKenzie T, Hoshino T, Tanaka T, Sueoka N (1986) The nucleotide sequence of pUB110: some salient features in relation to replication and its regulation. Plasmid 15: 93–103. 3010356

49. Carraro N, Poulin D, Burrus V (2015) Replication and Active Partition of Integrative and Conjugative Elements (ICEs) of the SXT/R391 Family: The Line between ICEs and Conjugative Plasmids Is Getting Thinner. PLoS Genet 11: e1005298. doi: 10.1371/journal.pgen.1005298 26061412

50. Lee CA, Thomas J, Grossman AD (2012) The Bacillus subtilis conjugative transposon ICEBs1 mobilizes plasmids lacking dedicated mobilization functions. J Bacteriol 194: 3165–3172. doi: 10.1128/JB.00301-12 22505685

51. Masai H, Arai K (1997) Frpo: a novel single-stranded DNA promoter for transcription and for primer RNA synthesis of DNA replication. Cell 89: 897–907. 9200608

52. Birch P, Khan SA (1992) Replication of single-stranded plasmid pT181 DNA in vitro. Proc Natl Acad Sci U S A 89: 290–294. 1729700

53. Kramer MG, Espinosa M, Misra TK, Khan SA (1999) Characterization of a single-strand origin, ssoU, required for broad host range replication of rolling-circle plasmids. Mol Microbiol 33: 466–475. 10417638

54. Kramer MG, Espinosa M, Misra TK, Khan SA (1998) Lagging strand replication of rolling-circle plasmids: specific recognition of the ssoA-type origins in different gram-positive bacteria. Proc Natl Acad Sci U S A 95: 10505–10510. 9724733

55. Kramer MG, Khan SA, Espinosa M (1997) Plasmid rolling circle replication: identification of the RNA polymerase-directed primer RNA and requirement for DNA polymerase I for lagging strand synthesis. EMBO J 16: 5784–5795. 9312036

56. Nomura N, Low RL, Ray DS (1982) Identification of ColE1 DNA sequences that direct single strand-to-double strand conversion by a phi X174 type mechanism. Proc Natl Acad Sci U S A 79: 3153–3157. 6212928

57. Guiney DG, Deiss C, Simnad V, Yee L, Pansegrau W, et al. (1989) Mutagenesis of the Tra1 core region of RK2 by using Tn5: identification of plasmid-specific transfer genes. J Bacteriol 171: 4100–4103. 2544570

58. Wilkins BM, Chatfield LK, Wymbs CC, Merryweather A (1985) Plasmid DNA primases and their role in bacterial conjugation. Basic Life Sci 30: 585–603. 3893412

59. Henderson D, Meyer RJ (1996) The primase of broad-host-range plasmid R1162 is active in conjugal transfer. J Bacteriol 178: 6888–6894. 8955311

60. Lanka E, Barth PT (1981) Plasmid RP4 specifies a deoxyribonucleic acid primase involved in its conjugal transfer and maintenance. J Bacteriol 148: 769–781. 6273381

61. Chatfield LK, Orr E, Boulnois GJ, Wilkins BM (1982) DNA primase of plasmid ColIb is involved in conjugal DNA synthesis in donor and recipient bacteria. J Bacteriol 152: 1188–1195. 6754700

62. Honda Y, Sakai H, Komano T, Bagdasarian M (1989) RepB' is required in trans for the two single-strand DNA initiation signals in oriV of plasmid RSF1010. Gene 80: 155–159. 2792769

63. Lin LS, Meyer RJ (1987) DNA synthesis is initiated at two positions within the origin of replication of plasmid R1162. Nucleic Acids Res 15: 8319–8331. 3313280

64. Wilkins BM, Boulnois GJ, Lanka E (1981) A plasmid DNA primase active in discontinuous bacterial DNA replication. Nature 290: 217–221. 7010183

65. Bron S (1990) Plasmids. In: Harwood CR, Cutting SM, editors. Molecular biological methods for Bacillus. Chhichester, UK: John Wiley & Sons, Ltd. pp. 75–175.

66. Fernández-López C, Bravo A, Ruiz-Cruz S, Solano-Collado V, Garsin DA, et al. (2014) Mobilizable Rolling-Circle Replicating Plasmids from Gram-Positive Bacteria: A Low-Cost Conjugative Transfer. Microbiol Spectrum 2: 8.

67. Perego M, Spiegelman GB, Hoch JA (1988) Structure of the gene for the transition state regulator, abrB: regulator synthesis is controlled by the spo0A sporulation gene in Bacillus subtilis. Mol Microbiol 2: 689–699. 3145384

68. Smith JL, Goldberg JM, Grossman AD (2014) Complete genome sequences of Bacillus subtilis subsp. subtilis laboratory strains JH642 (AG174) and AG1839. Genome Announc 2.

69. Bhavsar AP, Zhao X, Brown ED (2001) Development and characterization of a xylose-dependent system for expression of cloned genes in Bacillus subtilis: conditional complementation of a teichoic acid mutant. Appl Environ Microbiol 67: 403–410. 11133472

70. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA 3rd, et al. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343–345. doi: 10.1038/nmeth.1318 19363495

71. Horton RM, Hunt HD, Ho SN, Pullen JK, Pease LR (1989) Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene 77: 61–68. 2744488

72. Jaacks KJ, Healy J, Losick R, Grossman AD (1989) Identification and characterization of genes controlled by the sporulation-regulatory gene spo0H in Bacillus subtilis. J Bacteriol 171: 4121–4129. 2502532

73. Harwood CR, Cutting SM (1990) Molecular Biological Methods for Bacillus. Chichester: John Wiley & Sons.

74. Lemon KP, Grossman AD (1998) Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282: 1516–1519. 9822387

75. Lemon KP, Grossman AD (2000) Movement of replicating DNA through a stationary replisome. Mol Cell 6: 1321–1330. 11163206

76. Sambrook J, Fritsch EF, Maniatis T (1989) Moleculr cloning: a laboratory manual. New York: Cold Spring Laboratory Press.

77. Merrikh H, Machón C, Grainger WH, Grossman AD, Soultanas P (2011) Co-directional replication-transcription conflicts lead to replication restart. Nature 470: 554–557. doi: 10.1038/nature09758 21350489

78. Smits WK, Goranov AI, Grossman AD (2010) Ordered association of helicase loader proteins with the Bacillus subtilis origin of replication in vivo. Mol Microbiol 75: 452–461. doi: 10.1111/j.1365-2958.2009.06999.x 19968790

79. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402–408. 11846609

80. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410. 2231712

81. Bi D, Xu Z, Harrison EM, Tai C, Wei Y, et al. (2012) ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria. Nucleic Acids Res 40: D621–626. doi: 10.1093/nar/gkr846 22009673

82. Boe L, Gros MF, te Riele H, Ehrlich SD, Gruss A (1989) Replication origins of single-stranded-DNA plasmid pUB110. J Bacteriol 171: 3366–3372. 2722752

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