Bacterial replication, transcription and translation: Mechanistic insights from single-molecule biochemical studies

Nature Reviews Microbiology

Volumn 11, Issue 5, 2013, Pages 303-315

  Robinson, Andrew ^a   Van Oijen, Antoine M ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BACTERIAL ENZYME; BACTERIAL PROTEIN; DNA POLYMERASE; HELICASE; HOLOENZYME;

BACTERIAL KINETICS; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIOPHAGE; BIOCHEMISTRY; CHEMICAL REACTION; COMPLEX FORMATION; DNA REPLICATION; DNA TRANSCRIPTION; DNA TRANSLATION; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VITRO STUDY; MAGNETIC FIELD; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MYCOPLASMA GENITALIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA INTERACTION; PROTEIN PROCESSING; REPLISOME; REVIEW; SPECTROSCOPY;

BACTERIAL PHYSIOLOGICAL PHENOMENA; DNA REPLICATION; DNA, BACTERIAL; FLUORESCENCE RESONANCE ENERGY TRANSFER; PROTEIN BIOSYNTHESIS; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS);

EID: 84876420906     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro2994     Document Type: Review

References (81)

1. Bustamante, C., Cheng, W. & Mejia, Y. X. Revisiting the central dogma one molecule at a time. Cell 144, 480-497 (2011).
2. Browning, D. F. & Busby, S. J. The regulation of bacterial transcription initiation. Nature Rev. Microbiol. 2, 57-65 (2004).
3. Simonetti, A. et al. A structural view of translation initiation in bacteria. Cell. Mol. Life Sci. 66, 423-436 (2009).
4. Thanbichler, M. Synchronization of chromosome dynamics and cell division in bacteria. Cold Spring Harb. Perspect. Biol. 2, a000331 (2010).
5. Tinoco, I. Jr & Gonzalez, R. L. Jr. Biological mechanisms, one molecule at a time. Genes Dev. 25, 1205-1231 (2011).
6. Moore, P. B. How should we think about the ribosome? Annu. Rev. Biophys. 41, 1-19 (2012).
7. Dulin, D., Lipfert, J., Moolman, M. C. & Dekker, N. H. Studying genomic processes at the single-molecule level: introducing the tools and applications. Nature Rev. Genet. 14, 9-22 (2012).
8. Hamdan, S. M., Loparo, J. J., Takahashi, M., Richardson, C. C. & van Oijen, A. M. Dynamics of DNA replication loops reveal temporal control of lagging-strand synthesis. Nature 457, 336-339 (2009).
9. Vanzi, F., Broggio, C., Sacconi, L. & Pavone, F. S. Lac repressor hinge flexibility and DNA looping: single molecule kinetics by tethered particle motion. Nucleic Acids Res. 34, 3409-3420 (2006).
10. van Oijen, A. M. et al. Single-molecule kinetics of a; exonuclease reveal base dependence and dynamic disorder. Science 301, 1235-1238 (2003).
11. Lipfert, J., Wiggin, M., Kerssemakers, J. W., Pedaci, F. & Dekker, N. H. Freely orbiting magnetic tweezers to directly monitor changes in the twist of nucleic acids. Nature Commun. 2, 439 (2011).
12. Chen, C. et al. Single-molecule fluorescence measurements of ribosomal translocation dynamics. Mol. Cell 42, 367-377 (2011).
13. Mott, M. L. & Berger, J. M. DNA replication initiation: mechanisms and regulation in bacteria. Nature Rev. Microbiol. 5, 343-354 (2007).
14. Duderstadt, K. E., Chuang, K. & Berger, J. M. DNA stretching by bacterial initiators promotes replication origin opening. Nature 478, 209-213 (2011).
15. Zorman, S., Seitz, H., Sclavi, B. & Strick, T. R. Topological characterization of the DnaA-oriC complex using single-molecule nanomanipuation. Nucleic Acids Res. 40, 7375-7383 (2012).
16. Tanner, N. A. et al. E. coli DNA replication in the absence of free β clamps. EMBO J. 30, 1830-1840 (2011).
17. Robinson, A. et al. Essential biological processes of an emerging pathogen: DNA replication, transcription, and cell division in Acinetobacter spp. Microbiol. Mol. Biol. Rev. 74, 273-297 (2010).
18. Robinson, A., Causer, R. J. & Dixon, N. E. Architecture and conservation of the bacterial DNA replication machinery, an underexploited drug target. Curr. Drug Targets 13, 352-372 (2012).
19. Soultanas, P. Loading mechanisms of ring helicases at replication origins. Mol. Microbiol. 84, 6-16 (2012).
20. Zhang, Z. et al. Assembly of the bacteriophage T4 primosome: single-molecule and ensemble studies. Proc. Natl Acad. Sci. USA 102, 3254-3259 (2005).
21. Smiley, R. D., Zhuang, Z., Benkovic, S. J. & Hammes, G. G. Single-molecule investigation of the T4 bacteriophage DNA polymerase holoenzyme: multiple pathways of holoenzyme formation. Biochemistry 45, 7990-7997 (2006).
22. Tanner, N. A. et al. Real-time single-molecule observation of rolling-circle DNA replication. Nucleic Acids Res. 37, e27 (2009).
23. Dixon, N. E. DNA replication: prime-time looping. Nature 462, 854-855 (2009).
24. Manosas, M., Spiering, M. M., Zhuang, Z., Benkovic, S. J. & Croquette, V. Coupling DNA unwinding activity with primer synthesis in the bacteriophage T4 primosome. Nature Chem. Biol. 5, 904-912 (2009).
25. Pandey, M. et al. Coordinating DNA replication by means of priming loop and differential synthesis rate. Nature 462, 940-943 (2009).
26. Lee, J. B. et al. DNA primase acts as a molecular brake in DNA replication. Nature 439, 621-624 (2006).
27. Jergic, S. et al. The unstructured C-terminus of the τ subunit of Escherichia coli DNA polymerase III holoenzyme is the site of interaction with the α subunit. Nucleic Acids Res. 35, 2813-2824 (2007).
28. Lia, G., Michel, B. & Allemand, J. F. Polymerase exchange during Okazaki fragment synthesis observed in living cells. Science 335, 328-331 (2012).
29. Loparo, J. J., Kulczyk, A. W., Richardson, C. C. & van Oijen, A. M. Simultaneous single-molecule measurements of phage T7 replisome composition and function reveal the mechanism of polymerase exchange. Proc. Natl Acad. Sci. USA 108, 3584-3589 (2011).
30. Johnson, D. E., Takahashi, M., Hamdan, S. M., Lee, S. J. & Richardson, C. C. Exchange of DNA polymerases at the replication fork of bacteriophage T7. Proc. Natl Acad. Sci. USA 104, 5312-5317 (2007).
31. Reyes-Lamothe, R., Sherratt, D. J. & Leake, M. C. Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Science 328, 498-501 (2010).
32. McInerney, P., Johnson, A., Katz, F. & O'Donnell, M. Characterization of a triple DNA polymerase replisome. Mol. Cell 27, 527-538 (2007).
33. McHenry, C. S. DNA replicases from a bacterial perspective. Annu. Rev. Biochem. 80, 403-436 (2011).
34. Georgescu, R. E., Kurth, I. & O'Donnell, M. E. Single-molecule studies reveal the function of a third polymerase in the replisome. Nature Struct. Mol. Biol. 19, 113-116 (2012).
35. Gibb, B., Silverstein, T. D., Finkelstein, I. J. & Greene, E. C. Single-stranded DNA curtains for realtime single-molecule visualization of protein-nucleic acid interactions. Anal. Chem. 84, 7607-7612 (2012).
36. Merrikh, H., Zhang, Y., Grossman, A. D. & Wang, J. D. Replication-transcription conflicts in bacteria. Nature Rev. Microbiol. 10, 449-458 (2012).
37. Georgescu, R. E., Yao, N. Y. & O'Donnell, M. Singlemolecule analysis of the Escherichia coli replisome and use of clamps to bypass replication barriers. FEBS Lett. 584, 2596-2605 (2010).
38. Herbert, K. M., Greenleaf, W. J. & Block, S. M. Singlemolecule studies of RNA polymerase: motoring along. Annu. Rev. Biochem. 77, 149-176 (2008).
39. Larson, M. H., Landick, R. & Block, S. M. Singlemolecule studies of RNA polymerase: one singular sensation, every little step it takes. Mol. Cell 41, 249-262 (2011).
40. Kapanidis, A. N. et al. Initial transcription by RNA polymerase proceeds through a DNA-scrunching mechanism. Science 314, 1144-1147 (2006).
41. Revyakin, A., Liu, C., Ebright, R. H. & Strick, T. R. Abortive initiation and productive initiation by RNA polymerase involve DNA scrunching. Science 314, 1139-1143 (2006).
42. Frank, J. & Gonzalez, R. L. Jr. Structure and dynamics of a processive Brownian motor: the translating ribosome. Annu. Rev. Biochem. 79, 381-412 (2010).
43. Yu, J. & Oster, G. A small post-translocation energy bias aids nucleotide selection in T7 RNA polymerase transcription. Biophys. J. 102, 532-541 (2012).
44. Friedman, L. J. & Gelles, J. Mechanism of transcription initiation at an activator-dependent promoter defined by single-molecule observation. Cell 148, 679-689 (2012).
45. 70 in transcription elongation: singlemolecule analysis. Mol. Cell 20, 347-356 (2005).
46. Cordes, T. et al. Sensing DNA opening in transcription using quenchable Förster resonance energy transfer. Biochemistry 49, 9171-9180 (2010).
47. Chakraborty, A. et al. Opening and closing of the bacterial RNA polymerase clamp. Science 337, 591-595 (2012).
48. Sekine, S., Tagami, S. & Yokoyama, S. Structural basis of transcription by bacterial and eukaryotic RNA polymerases. Curr. Opin. Struct. Biol. 22, 110-118 (2012).
49. Hartzog, G. A. & Kaplan, C. D. Competing for the clamp: promoting RNA polymerase processivity and managing the transition from initiation to elongation. Mol. Cell 43, 161-163 (2011).
50. Tagami, S. et al. Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein. Nature 468, 978-982 (2010).
51. Aitken, C. E., Petrov, A. & Puglisi, J. D. Single ribosome dynamics and the mechanism of translation. Annu. Rev. Biophys. 39, 491-513 (2010).
52. Blanchard, S. C. Single-molecule observations of ribosome function. Curr. Opin. Struct. Biol. 19, 103-109 (2009).
53. Laursen, B. S., Sorensen, H. P., Mortensen, K. K. & Sperling-Petersen, H. U. Initiation of protein synthesis in bacteria. Microbiol. Mol. Biol. Rev. 69, 101-123 (2005).
54. Milon, P. et al. The ribosome-bound initiation factor 2 recruits initiator tRNA to the 30S initiation complex. EMBO Rep. 11, 312-316 (2010).
55. Milon, P., Maracci, C., Filonava, L., Gualerzi, C. O. & Rodnina, M. V. Real-time assembly landscape of bacterial 30S translation initiation complex. Nature Struct. Mol. Biol. 19, 609-615 (2012).
56. Milon, P. & Rodnina, M. V. Kinetic control of translation initiation in bacteria. Crit. Rev. Biochem. Mol. Biol. 47, 334-348 (2012).
57. Tsai, A. et al. Heterogeneous pathways and timing of factor departure during translation initiation. Nature 487, 390-393 (2012).
58. Caldas, T., Laalami, S. & Richarme, G. Chaperone properties of bacterial elongation factor EF-G and initiation factor IF2. J. Biol. Chem. 275, 855-860 (2000).
59. Ban, N., Nissen, P., Hansen, J., Moore, P. B. & Steitz, T. A. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289, 905-920 (2000).
60. Uemura, S. et al. Real-time tRNA transit on single translating ribosomes at codon resolution. Nature 464, 1012-1017 (2010).
61. Chen, C. et al. Allosteric versus spontaneous exit-site (E-site) tRNA dissociation early in protein synthesis. Proc. Natl Acad. Sci. USA 108, 16980-16985 (2011).
62. Karr, J. R. et al. A whole-cell computational model predicts phenotype from genotype. Cell 150, 389-401 (2012).
63. Choi, P. J., Cai, L., Frieda, K. & Xie, X. S. A stochastic single-molecule event triggers phenotype switching of a bacterial cell. Science 322, 442-446 (2008).
64. Li, G. W. & Xie, X. S. Central dogma at the singlemolecule level in living cells. Nature 475, 308-315 (2011).
65. Taniguchi, Y. et al. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329, 533-538 (2010).
66. Levene, M. J. et al. Zero-mode waveguides for singlemolecule analysis at high concentrations. Science 299, 682-686 (2003).
67. Loveland, A. B., Habuchi, S., Walter, J. C. & van Oijen, A. M. A general approach to break the concentration barrier in single-molecule imaging. Nature Methods 9, 987-992 (2012).
68. Aitken, C. E. & Puglisi, J. D. Following the intersubunit conformation of the ribosome during translation in real time. Nature Struct. Mol. Biol. 17, 793-800 (2010).
69. Altuntop, M. E., Ly, C. T. & Wang, Y. Single-molecule study of ribosome hierarchic dynamics at the peptidyl transferase center. Biophys. J. 99, 3002-3009 (2010).
70. Feldman, M. B., Terry, D. S., Altman, R. B. & Blanchard, S. C. Aminoglycoside activity observed on single pre-translocation ribosome complexes. Nature Chem. Biol. 6, 54-62 (2010).
71. Ly, C. T., Altuntop, M. E. & Wang, Y. Single-molecule study of viomycin's inhibition mechanism on ribosome translocation. Biochemistry 49, 9732-9738 (2010).
72. Munro, J. B., Wasserman, M. R., Altman, R. B., Wang, L. & Blanchard, S. C. Correlated conformational events in EF-G and the ribosome regulate translocation. Nature Struct. Mol. Biol. 17, 1470-1477 (2010).
73. Wang, L. et al. Allosteric control of the ribosome by small-molecule antibiotics. Nature Struct. Mol. Biol. 19, 957-963 (2012).
74. Nelson, S. W. & Benkovic, S. J. Response of the bacteriophage T4 replisome to noncoding lesions and regression of a stalled replication fork. J. Mol. Biol. 401, 743-756 (2010).
75. Yao, N. Y., Georgescu, R. E., Finkelstein, J. & O'Donnell, M. E. Single-molecule analysis reveals that the lagging strand increases replisome processivity but slows replication fork progression. Proc. Natl Acad. Sci. USA 106, 13236-13241 (2009).
76. Badrinarayanan, A., Reyes-Lamothe, R., Uphoff, S., Leake, M. C. & Sherratt, D. J. In vivo architecture and action of bacterial structural maintenance of chromosome proteins. Science 338, 528-531 (2012).
77. Lia, G. et al. RecA-promoted, RecFOR-independent progressive disassembly of replisomes stalled by helicase inactivation. Mol. Cell 49, 547-557 (2012).
78. Etson, C. M., Hamdan, S. M., Richardson, C. C. & van Oijen, A. M. Thioredoxin suppresses microscopic hopping of T7 DNA polymerase on duplex DNA. Proc. Natl Acad. Sci. USA 107, 1900-1905 (2010).
79. Sinha, N. K., Morris, C. F. & Alberts, B. M. Efficient in vitro replication of double-stranded DNA templates by a purified T4 bacteriophage replication system. J. Biol. Chem. 255, 4290-4293 (1980).
80. Qu, X. et al. The ribosome uses two active mechanisms to unwind messenger RNA during translation. Nature 475, 118-121 (2011).
81. Tang, G. Q., Roy, R., Bandwar, R. P., Ha, T. & Patel, S. S. Real-time observation of the transition from transcription initiation to elongation of the RNA polymerase. Proc. Natl Acad. Sci. USA 106, 22175-22180 (2009).