DNA motifs that sculpt the bacterial chromosome

Nature Reviews Microbiology

Volumn 9, Issue 1, 2011, Pages 15-26

  Touzain, Fabrice ^a   Petit, Marie Agnés ^a   Schbath, Sophie ^b   Karoui, Meriem E ^a  

^a UMR1319 MICALIS   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL CHROMOSOME; BINDING SITE; CELL DIVISION; CELL REGENERATION; CELLULAR DISTRIBUTION; CHROMOSOMAL PARAMETERS; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; DAUGHTER CELL; DNA BINDING MOTIF; DNA SEQUENCE; DNA TRANSFECTION; ESCHERICHIA COLI; GENE CLUSTER; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

BASE SEQUENCE; CHROMOSOMES, BACTERIAL; DNA REPAIR; DNA REPLICATION; DNA, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL;

BACTERIA (MICROORGANISMS);

EID: 78650270761     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2477     Document Type: Review

References (118)

1. Reyes-Lamothe, R., Wang, X. & Sherratt, D. Escherichia coli and its chromosome. Trends Microbiol. 16, 238-245 (2008).
2. Katayama, T., Ozaki, S., Keyamura, K. & Fujimitsu, K. Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nature Rev. Microbiol. 8, 163-170 (2010).
3. Michel, B., Boubakri, H., Baharoglu, Z., LeMasson, M. & Lestini, R. Recombination proteins and rescue of arrested replication forks. DNA Repair 6, 967-980 (2007).
4. Dillingham, M. S. & Kowalczykowski, S. C. RecBCD enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 72, 642-671 (2008).
5. Duggin, I. G., Wake, R. G., Bell, S. D. & Hill, T. M. The replication fork trap and termination of chromosome replication. Mol. Microbiol. 70, 1323-1333 (2008).
6. Bigot, S., Sivanathan, V., Possoz, C., Barre, F. X. & Cornet, F. FtsK, a literate chromosome segregation machine. Mol. Microbiol. 64, 1434-1441 (2007).
7. Espeli, O., Mercier, R. & Boccard, F. DNA dynamics vary according to macrodomain topography in the, E. coli chromosome. Mol. Microbiol. 68, 1418-1427 (2008).
8. D'Haeseleer, P. What are DNA sequence motifs? Nature Biotech. 24, 423-425 (2006).
9. Dillon, S. C. & Dorman, C. J. Bacterial nucleoid-associated proteins, nucleoid structure and gene expression. Nature Rev. Microbiol. 8, 185-195 (2010).
10. Matsui, M., Oka, A., Takanami, M., Yasuda, S. & Hirota, Y. Sites of dnaA protein-binding in the replication origin of the Escherichia coli K?12 chromosome. J. Mol. Biol. 184, 529-533 (1985).
11. Fuller, R. S., Funnell, B. E. & Kornberg, A. The dnaA protein complex with the E. coli chromosomal replication origin (oriC) and other DNA sites. Cell 38, 889-900 (1984).
12. Messer, W. The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS Microbiol. Rev. 26, 355-374 (2002).
13. Fukuoka, T., Moriya, S., Yoshikawa, H. & Ogasawara, N. Purification and characterization of an initiation protein for chromosomal replication, DnaA, in Bacillus subtilis. J. Biochem. 107, 732-739 (1990).
14. Mackiewicz, P., Zakrzewska-Czerwinska, J., Zawilak, A., Dudek, M. R. & Cebrat, S. Where does bacterial replication start Rules for predicting the oriC region. Nucleic Acids Res. 32, 3781-3791 (2004).
15. Ishikawa, S. et al. Distribution of stable DnaA-binding sites on the Bacillus subtilis genome detected using a modified ChIP-chip method. DNA Res. 14, 155-168 (2007).
16. Roth, A. & Messer, W. High-affinity binding sites for the initiator protein DnaA on the chromosome of Escherichia coli. Mol. Microbiol. 28, 395-401 (1998).
17. Boye, E., Lobner-Olesen, A. & Skarstad, K. Limiting DNA replication to once and only once. EMBO Rep. 1, 479-483 (2000).
18. Ogawa, T., Yamada, Y., Kuroda, T., Kishi, T. & Moriya, S. The datA locus predominantly contributes to the initiator titration mechanism in the control of replication initiation in Escherichia coli. Mol. Microbiol. 44, 1367-1375 (2002).
19. Fujimitsu, K., Senriuchi, T. & Katayama, T. Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA. Genes Dev. 23, 1221-1233 (2009).
20. Messer, W. & Weigel, C. DnaA initiator - also a transcription factor. Mol. Microbiol. 24, 1-6 (1997).
21. Goranov, A. I., Katz, L., Breier, A. M., Burge, C. B. & Grossman, A. D. A transcriptional response to replication status mediated by the conserved bacterial replication protein DnaA. Proc. Natl Acad. Sci. USA 102, 12932-12937 (2005).
22. 6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nature Rev. Microbiol. 4, 183-192 (2006).
23. Slater, S. et al. E. coli SeqA protein binds oriC in two different methyl-modulated reactions appropriate to its roles in DNA replication initiation and origin sequestration. Cell 82, 927-936 (1995).
24. Brendler, T., Sawitzke, J., Sergueev, K. & Austin, S. A case for sliding SeqA tracts at anchored replication forks during Escherichia coli chromosome replication and segregation. EMBO J. 19, 6249-6258 (2000).
25. Fossum, S., Crooke, E. & Skarstad, K. Organization of sister origins and replisomes during multifork DNA replication in Escherichia coli. EMBO J. 26, 4514-4522 (2007).
26. Schofield, M. J. & Hsieh, P. DNA mismatch repair: molecular mechanisms and biological function. Annu. Rev. Microbiol. 57, 579-608 (2003).
27. Marinus, M. G. & Casadesus, J. Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. FEMS Microbiol. Rev. 33, 488-503 (2009).
28. Henaut, A., Rouxel, T., Gleizes, A., Moszer, I. & Danchin, A. Uneven distribution of GATC motifs in the Escherichia coli chromosome, its plasmids and its phages. J. Mol. Biol. 257, 574-585 (1996).
29. Sanchez-Romero, M. A. et al. Dynamic distribution of SeqA protein across the chromosome of Escherichia coli K?12. mBio 1, e00012-10 (2010).
30. Collier, J., McAdams, H. H. & Shapiro, L. A DNA methylation ratchet governs progression through a bacterial cell cycle. Proc. Natl Acad. Sci. USA 104, 17111-17116 (2007).
31. Reisenauer, A. & Shapiro, L. DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter. EMBO J. 21, 4969-4977 (2002).
32. Kaplan, D. L. & Bastia, D. Mechanisms of polar arrest of a replication fork. Mol. Microbiol. 72, 279-285 (2009).
33. Duggin, I. G. & Bell, S. D. Termination structures in the Escherichia coli chromosome replication fork trap. J. Mol. Biol. 387, 532-539 (2009).
34. Wake, R. G. Replication fork arrest and termination of chromosome replication in Bacillus subtilis. FEMS Microbiol. Lett. 153, 247-254 (1997).
35. Stahl, F. W. Chi: A little sequence controls a big enzyme. Genetics 170, 487-493 (2005).
36. Handa, N., Ohashi, S., Kusano, K. & Kobayashi, I. Chi-star, a chi-related 11-mer sequence partially active in an E. coli recC1004 strain. Genes Cells 2, 525-536 (1997).
37. Singleton, M. R., Dillingham, M. S., Gaudier, M., Kowalczykowski, S. C. & Wigley, D. B. Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 432, 187-193 (2004).
38. Dixon, D. A. & Kowalczykowski, S. C. The recombination hotspot χ is a regulatory sequence that acts by attenuating the nuclease activity of the E. coli RecBCD enzyme. Cell 73, 87-96 (1993).
39. Kooistra, J., Haijema, B. J. & Venema, G. The Bacillus subtilis addAB genes are fully functional in Escherichia coli. Mol. Microbiol. 7, 915-923 (1993).
40. El Karoui, M., Ehrlich, D. & Gruss, A. Identification of the lactococcal exonuclease/recombinase and its modulation by the putative Chi sequence. Proc. Natl Acad. Sci. USA 95, 626-631 (1998).
41. Sinha, K. M., Unciuleac, M. C., Glickman, M. S. & Shuman, S. AdnAB: a new DSB-resecting motor-nuclease from mycobacteria. Genes Dev. 23, 1423-1437 (2009).
42. Rocha, E. P., Cornet, E. & Michel, B. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet. 1, e15 (2005).
43. Cromie, G. A. Phylogenetic ubiquity and shuffling of the bacterial RecBCD and AddAB recombination complexes. J. Bacteriol. 191, 5076-5084 (2009).
44. Kuzminov, A. Collapse and repair of replication forks in Escherichia coli. Mol. Microbiol. 16, 373-384 (1995).
45. Viollier, P. H. et al. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc. Natl Acad. Sci. USA 101, 9257-9262 (2004).
46. Wu, L. J. & Errington, J. Use of asymmetric cell division and spoIIIE mutants to probe chromosome orientation and organization in Bacillus subtilis. Mol. Microbiol. 27, 777-786 (1998).
47. Niki, H., Yamaichi, Y. & Hiraga, S. Dynamic organization of chromosomal DNA in Escherichia coli. Genes Dev. 14, 212-223 (2000).
48. Valens, M., Penaud, S., Rossignol, M., Cornet, F. & Boccard, F. Macrodomain organization of the Escherichia coli chromosome. EMBO J. 23, 4330-4341 (2004).
49. Lin, D. C. & Grossman, A. D. Identification and characterization of a bacterial chromosome partitioning site. Cell 92, 675-685 (1998).
50. Gerdes, K., Howard, M. & Szardenings, F. Pushing and pulling in prokaryotic DNA segregation. Cell 141, 927-942 (2010).
51. Gruber, S. & Errington, J. Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137, 685-696 (2009).
52. Sullivan, N. L., Marquis, K. A. & Rudner, D. Z. Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137, 697-707 (2009).
53. Breier, A. M. & Grossman, A. D. Whole-genome analysis of the chromosome partitioning and sporulation protein Spo0J (ParB) reveals spreading and origin-distal sites on the Bacillus subtilis chromosome. Mol. Microbiol. 64, 703-718 (2007).
54. Livny, J., Yamaichi, Y. & Waldor, M. K. Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J. Bacteriol. 189, 8693-8703 (2007).
55. Toro, E., Hong, S. H., McAdams, H. H. & Shapiro, L. Caulobacter requires a dedicated mechanism to initiate chromosome segregation. Proc. Natl Acad. Sci. USA 105, 15435-15440 (2008).
56. Fogel, M. A. & Waldor, M. K. A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes Dev. 20, 3269-3282 (2006).
57. Yamaichi, Y., Fogel, M. A., Mcleod, S. M., Hui, M. P. & Waldor, M. K. Distinct centromere-like parS sites on the two chromosomes of Vibrio species. J. Bacteriol. 189, 5314-5324 (2007).
58. Saint-Dic, D., Frushour, B. P., Kehrl, J. H. & Kahng, L. S. A parA homolog selectively influences positioning of the large chromosome origin in Vibrio cholerae. J. Bacteriol. 188, 5626-5631 (2006).
59. Shebelut, C. W., Jensen, R. B. & Gitai, Z. Growth conditions regulate the requirements for Caulobacter chromosome segregation. J. Bacteriol. 191, 1097-1100 (2009).
60. Yamaichi, Y. & Niki, H. migS, a cis-acting site that affects bipolar positioning of oriC on the Escherichia coli chromosome. EMBO J. 23, 221-233 (2004).
61. Fekete, R. A. & Chattoraj, D. K. A cis-acting sequence involved in chromosome segregation in Escherichia coli. Mol. Microbiol. 55, 175-183 (2005).
62. Ben-Yehuda, S. et al. Defining a centromere-like element in Bacillus subtilis by identifying the binding sites for the chromosome-anchoring protein RacA. Mol. Cell 17, 773-782 (2005).
63. Wu, L. J. & Errington, J. RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol. Microbiol. 49, 1463-1475 (2003).
64. Ben-Yehuda, S., Rudner, D. Z. & Losick, R. RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299, 532-536 (2003).
65. Steiner, W. W. & Kuempel, P. L. Cell division is required for resolution of dimer chromosomes at the dif locus of Escherichia coli. Mol. Microbiol. 27, 257-268 (1998).
66. Perals, K., Cornet, F., Merlet, Y., Delon, I. & Louarn, J. M. 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 (2000).
67. Bigot, S. et al. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J. 24, 3770-3780 (2005).
68. Levy, O. et al. Identification of oligonucleotide sequences that direct the movement of the Escherichia coli FtsK translocase. Proc. Natl Acad. Sci. USA 102, 17618-17623 (2005).
69. Sivanathan, V. et al. KOPS-guided DNA translocation by FtsK safeguards Escherichia coli chromosome segregation. Mol. Microbiol. 71, 1031-1042 (2009).
70. Sivanathan, V. et al. The FtsK γ domain directs oriented DNA translocation by interacting with KOPS. Nature Struct. Mol. Biol. 13, 965-972 (2006).
71. Lowe, J. et al. Molecular mechanism of sequence-directed DNA loading and translocation by FtsK. Mol. Cell 31, 498-509 (2008).
72. Biller, S. J. & Burkholder, W. F. The Bacillus subtilis SftA (YtpS) and SpoIIIE DNA translocases play distinct roles in growing cells to ensure faithful chromosome partitioning. Mol. Microbiol. 74, 790-809 (2009).
73. Kaimer, C., González-Pastor, J. E. E. & Graumann, P. L. SpoIIIE and a novel type of DNA translocase, SftA, couple chromosome segregation with cell division in Bacillus subtilis. Mol. Microbiol. 74, 810-825 (2009).
74. Sharpe, M. E. & Errington, J. The Bacillus subtilis soj-spo0J locus is required for a centromere-like function involved in prespore chromosome partitioning. Mol. Microbiol. 21, 501-509 (1996).
75. Bath, J., Wu, L. J., Errington, J. & Wang, J. C. Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290, 995-997 (2000).
76. Wu, L. J. & Errington, J. Bacillus subtilis SpoIIIE protein required for DNA segregation during asymmetric cell division. Science 264, 572-575 (1994).
77. Ptacin, J. L. et al. Sequence-directed DNA export guides chromosome translocation during sporulation in Bacillus subtilis. Nature Struct. Mol. Biol. 15, 485-493 (2008).
78. Hendrickson, H. & Lawrence, J. G. Selection for chromosome architecture in bacteria. J. Mol. Evol. 62, 615-629, (2006).
79. Salzberg, S. L., Salzberg, A. J., Kerlavage, A. R. & Tomb, J. F. Skewed oligomers and origins of replication. Gene 217, 57-67 (1998).
80. Mercier, R. et al. The MatP/matS site-specific system organizes the terminus region of the, E. coli chromosome into a macrodomain. Cell 135, 475-485 (2008).
81. Wu, L. J. & Errington, J. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 11 7, 915-925 (2004).
82. Wu, L. J. et al. Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J. 28, 1940-1952 (2009).
83. Bernhardt, T. G. & de Boer, P. A. SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18, 555-564 (2005).
84. Danner, D. B., Deich, R. A., Sisco, K. L. & Smith, H. O. An eleven-base-pair sequence determines the specificity of DNA uptake in Haemophilus transformation. Gene 11, 311-318 (1980).
85. Goodman, S. D. & Scocca, J. J. Identification and arrangement of the DNA sequence recognized in specific transformation of Neisseria gonorrhoeae. Proc. Natl Acad. Sci. USA 85, 6982-6986 (1988).
86. Smith, H. O., Gwinn, M. L. & Salzberg, S. L. DNA uptake signal sequences in naturally transformable bacteria. Res. Microbiol. 150, 603-616 (1999).
87. Kingsford, C. L., Ayanbule, K. & Salzberg, S. L. Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol. 8, R22 (2007).
88. El Karoui, M., Biaudet, V., Schbath, S. & Gruss, A. Characteristics of Chi distribution on different bacterial genomes. Res. Microbiol. 150, 579-587 (1999).
89. Uno, R., Nakayama, Y. & Tomita, M. Over-representation of Chi sequences caused by di-codon increase in Escherichia coli K-12. Gene 380, 30-37 (2006).
90. Colbert, T., Taylor, A. F. & Smith, G. R. Genomics, Chi sites and codons: 'islands of preferred DNA pairing' are oceans of ORFs. Trends Genet. 14, 485-488 (1998).
91. Biaudet, V., El Karoui, M. & Gruss, A. Codon usage can explain GT-rich islands surrounding Chi sites on the Escherichia coli genome. Mol. Microbiol. 29, 666-669 (1998).
92. Bakkali, M. Genome dynamics of short oligonucleotides: the example of bacterial DNA uptake enhancing sequences. PLoS ONE 2, e741 (2007).
93. Sourice, S., Biaudet, V., El Karoui, M., Ehrlich, S. D. & Gruss, A. Identification of the Chi site of Haemophilus influenzae as several sequences related to the Escherichia coli Chi site. Mol. Microbiol. 27, 1021-1029 (1998).
94. Phillips, G. J., Arnold, J. & Ivarie, R. The effect of codon usage on the oligonucleotide composition of the E. coli genome and identification of over- and underrepresented sequences by Markov chain analysis. Nucleic Acids Res. 15, 2627-2638 (1987).
95. Lobry, J. R. Asymmetric substitution patterns in the two DNA strands of bacteria. Mol. Biol. Evol. 13, 660-665 (1996).
96. Mrazek, J. Finding sequence motifs in prokaryotic genomes - a brief practical guide for a microbiologist. Brief Bioinform. 10, 525-536 (2009).
97. Riva, A. et al. Characterization of the GATC regulatory network in E. coli. BMC Genomics 5, 48 (2004).
98. Halpern, D. et al. Identification of DNA motifs implicated in maintenance of bacterial core genomes by predictive modeling. PLoS Genet. 3, 1614-1621 (2007).
99. Lawrence, J. G. & Hendrickson, H. Lateral gene transfer: when will adolescence end? Mol. Microbiol. 50, 739-749 (2003).
100. Treangen, T. J., Ambur, O. H., Tonjum, T. & Rocha, E. P. The impact of the neisserial DNA uptake sequences on genome evolution and stability. Genome Biol. 9, R60 (2008).
101. Redfield, R. J. et al. Evolution of competence and DNA uptake specificity in the Pasteurellaceae. BMC Evol. Biol. 6, 82 (2006).
102. Hayashi, T. et al. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 8, 11-22 (2001).
103. Eisen, J. A., Heidelberg, J. F., White, O. & Salzberg, S. L. Evidence for symmetric chromosomal inversions around the replication origin in bacteria. Genome Biol. 1, RESEARCH0011 (2000).
104. Rocha, E. P. C. The organization of the bacterial genome. Annu. Rev. Genet. 42, 211-233 (2008).
105. Darling, A. E., Miklos, I. & Ragan, M. A. Dynamics of genome rearrangement in bacterial populations. PLoS Genet. 4, e1000128 (2008).
106. Atlas, J. C., Nikolaev, E. V., Browning, S. T. & Shuler, M. L. Incorporating genome-wide DNA sequence information into a dynamic whole-cell model of Escherichia coli: application to DNA replication. IET Syst. Biol. 2, 369-382 (2008).
107. Robin, S., Rodophe, F. & Schbath, S. DNA, Words and Models (Cambridge Univ. Press, Cambridge, UK, 2005).
108. Roquain, E. & Schbath, S. Improved compound Poisson approximation for the number of multiple words in a stationary Markov chain. Adv. Appl. Probab. 39, 1-13 (2007).
109. Nuel, G. LD-SPatt: large deviations statistics for patterns on Markov chains. J. Comput. Biol. 11, 1023-1033 (2004).
110. Behrens, S. & Lowe, M. Moderate deviations for word counts in biological sequences. J. Appl. Probab. 46, 1020-1037 (2009).
111. Robin, S., Schbath, S. & Vandewalle, V. Statistical tests to compare motif count exceptionalities. BMC Bioinformatics 8, 84 (2007).
112. Karlin, S. & Macken, C. Some statistical problems in the assessment of inhomogeneities of DNA sequence data. J. Am. Stat. Assoc. 86, 27-35 (1991).
113. Robin, S. A compound Poisson model for word occurences in DNA sequences. J. R. Stat. Soc. Ser. C Appl. Stat. 51, 437-451 (2002).
114. Schbath, S. & Hoebeke, M. in Genome?Scale Pattern Analysis in the Post?ENCODE Era (eds Elnitski, L., Piontkivska, H. & Welch, L. E.) (Word Scientific, in the press).
115. Nuel, G. S-SPatt: simple statistics for patterns on Markov chains. Bioinformatics 21, 3051-3052 (2005).
116. Mrazek, J., Xie, S., Guo, X. & Srivastava, A. AIMIE: a web-based environment for detection and interpretation of significant sequence motifs in prokaryotic genomes. Bioinformatics 24, 1041-1048 (2008).
117. Thomas-Chollier, M. et al. RSAT: regulatory sequence analysis tools. Nucleic Acids Res. 36, W119-W127 (2008).
118. Hertz, G. Z. & Stormo, G. D. Identifying DNA and protein patterns with statistically significant alignments of multiple sequences. Bioinformatics 15, 563-577 (1999).