Tracking of chromosome dynamics in live Streptococcus pneumoniae reveals that transcription promotes chromosome segregation

Molecular Microbiology

Volumn 91, Issue 6, 2014, Pages 1088-1105

  Kjos, Morten ^a   Veening, Jan Willem ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; PROTEIN SMC; RIFAMPICIN; STREPTOLYDIGIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CHROMOSOME; CELL CYCLE; CHROMOSOME ABERRATION; CHROMOSOME ANALYSIS; CHROMOSOME SEGREGATION; CONTROLLED STUDY; DNA MODIFICATION; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTION ELONGATION; TRANSCRIPTION REGULATION;

BACTERIA (MICROORGANISMS); STREPTOCOCCUS PNEUMONIAE;

CELL CYCLE; CHROMOSOME SEGREGATION; MICROSCOPY, FLUORESCENCE; STREPTOCOCCUS PNEUMONIAE; TIME-LAPSE IMAGING; TRANSCRIPTION, GENETIC;

EID: 84896714120     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12517     Document Type: Article

References (76)

1. Avery, O.T., Macleod, C.M., and McCarty, M. (1944) Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a deoxyribonucleic acid fraction isolated from pneumococcus type III. J Exp Med 79: 137-158.
2. Baker, T.A., and Kornberg, A. (1988) Transcriptional activation of initiation of replication from the E.coli chromosomal origin: an RNA-DNA hybrid near oriC. Cell 55: 113-123.
3. Bates, D., and Kleckner, N. (2005) Chromosome and replisome dynamics in E.coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121: 899-911.
4. Beilharz, K., Nováková, L., Fadda, D., Branny, P., Massidda, O., and Veening, J.-W. (2012) Control of cell division in Streptococcus pneumoniae by the conserved Ser/Thr protein kinase StkP. Proc Natl Acad Sci USA 109: E905-E913.
5. Bernhardt, T.G., and de Boer, P.A.J. (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E.coli. Mol Cell 18: 555-564.
6. Bloom, K., and Joglekar, A. (2010) Towards building a chromosome segregation machine. Nature 463: 446-456.
7. Le Bourgeois, P., Bugarel, M., Campo, N., Daveran-Mingot, M.-L., Labonté, J., Lanfranchi, D., etal. (2007) The unconventional Xer recombination machinery of Streptococci/Lactococci. PLoS Genet 3: e117.
8. Britton, R.A., Lin, D.C., and Grossman, A.D. (1998) Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12: 1254-1259.
9. Cabrera, J.E., Cagliero, C., Quan, S., Squires, C.L., and Jin, D.J. (2009) Active transcription of rRNA operons condenses the nucleoid in Escherichia coli: examining the effect of transcription on nucleoid structure in the absence of transertion. J Bacteriol 191: 4180-4185.
10. Campbell, E.A., Korzheva, N., Mustaev, A., Murakami, K., Nair, S., Goldfarb, A., and Darst, S.A. (2001) Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104: 901-912.
11. Clewell, D.B., and Evenchik, B.G. (1973) Effects of rifampicin, streptolydigin and actinomycin D on the replication of Col E1 plasmid DNA in Escherichia coli. J Mol Biol 75: 503-513.
12. Couturier, E., and Rocha, E.P.C. (2006) Replication-associated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Mol Microbiol 59: 1506-1518.
13. Danilova, O., Reyes-Lamothe, R., Pinskaya, M., Sherratt, D., and Possoz, C. (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.
14. Dasgupta, S., Maisnier-Patin, S., and Nordstrom, K. (2000) New genes with old modus operandi: the connection between supercoiling and partitioning of DNA in Escherichia coli. EMBO Rep 1: 323-327.
15. Drlica, K., and Rouviere-Yaniv, J. (1987) Histonelike proteins of bacteria. Microbiol Rev 51: 301-319.
16. Dworkin, J., and Losick, R. (2002) Does RNA polymerase help drive chromosome segregation in bacteria? Proc Natl Acad Sci USA 99: 14089-14094.
17. Fisher, J.K., Bourniquel, A., Witz, G., Weiner, B., Prentiss, M., and Kleckner, N. (2013) Four-dimensional imaging of E.coli nucleoid organization and dynamics in living cells. Cell 153: 882-895.
18. Gelles, J., and Landick, R. (1998) RNA polymerase as a molecular motor. Cell 93: 13-16.
19. Gitai, Z., Dye, N.A., Reisenauer, A., Wachi, M., and Shapiro, L. (2005) MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120: 329-341.
20. Graumann, P., Losick, R., and Strunnikov, A.V. (1998) Subcellular localization of Bacillus subtilis SMC, a protein involved in chromosome condensation and segregation. J Bacteriol 180: 5749-5755.
21. Gruber, S., and Errington, J. (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B.subtilis. Cell 137: 685-696.
22. Holmes, V.F., and Cozzarelli, N.R. (2000) Closing the ring: links between SMC proteins and chromosome partitioning, condensation, and supercoiling. Proc Natl Acad Sci USA 97: 1322-1324.
23. Ireton, K., Gunther, N.W., 4th, and Grossman, A.D. (1994) spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176: 5320-5329.
24. Jin, D.J., and Cabrera, J.E. (2006) Coupling the distribution of RNA polymerase to global gene regulation and the dynamic structure of the bacterial nucleoid in Escherichia coli. J Struct Biol 156: 284-291.
25. de Jong, I.G., Beilharz, K., Kuipers, O.P., and Veening, J.-W. (2011) Live Cell Imaging of Bacillus subtilis and Streptococcus pneumoniae using Automated Time-lapse Microscopy. J Vis Exp 53: pii:3145. doi: 10.3791/3145
26. Joshi, M.C., Bourniquel, A., Fisher, J., Ho, B.T., Magnan, D., Kleckner, N., and Bates, D. (2011) Escherichia coli sister chromosome separation includes an abrupt global transition with concomitant release of late-splitting intersister snaps. Proc Natl Acad Sci USA 108: 2765-2770.
27. Jun, S., and Mulder, B. (2006) Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proc Natl Acad Sci USA 103: 12388-12393.
28. Jun, S., and Wright, A. (2010) Entropy as the driver of chromosome segregation. Nat Rev Microbiol 8: 600-607.
29. Junier, I., Boccard, F., and Espéli, O. (2013) Polymer modeling of the E.coli genome reveals the involvement of locus positioning and macrodomain structuring for the control of chromosome conformation and segregation. Nucleic Acids Res. doi: 10.1093/nar/gkt1005
30. Khodursky, A.B., Peter, B.J., Schmid, M.B., DeRisi, J., Botstein, D., Brown, P.O., and Cozzarelli, N.R. (2000) Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc Natl Acad Sci USA 97: 9419-9424.
31. Kruse, T., Blagoev, B., Løbner-Olesen, A., Wachi, M., Sasaki, K., Iwai, N., etal. (2006) Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev 20: 113-124.
32. Land, A.D., Tsui, H.-C.T., Kocaoglu, O., Vella, S.A., Shaw, S.L., Keen, S.K., etal. (2013) Requirement of essential Pbp2x and GpsB for septal ring closure in Streptococcus pneumoniae D39. Mol Microbiol 90: 939-955.
33. Lanie, J.A., Ng, W.-L., Kazmierczak, K.M., Andrzejewski, T.M., Davidsen, T.M., Wayne, K.J., etal. (2007) Genome sequence of Avery's virulent serotype 2 strain D39 of Streptococcus pneumoniae and comparison with that of unencapsulated laboratory strain R6. J Bacteriol 189: 38-51.
34. Laptenko, O., Lee, J., Lomakin, I., and Borukhov, S. (2003) Transcript cleavage factors GreA and GreB act as transient catalytic components of RNA polymerase. EMBO J 22: 6322-6334.
35. Le, T.B.K., Imakaev, M.V., Mirny, L.A., and Laub, M.T. (2013) High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342: 731-734.
36. Lemon, K.P., and Grossman, A.D. (2001) The extrusion-capture model for chromosome partitioning in bacteria. Genes Dev 15: 2031-2041.
37. Lewis, P.J., Thaker, S.D., and Errington, J. (2000) Compartmentalization of transcription and translation in Bacillus subtilis. EMBO J 19: 710-718.
38. Libby, E.A., Roggiani, M., and Goulian, M. (2012) Membrane protein expression triggers chromosomal locus repositioning in bacteria. Proc Natl Acad Sci USA 109: 7445-7450.
39. Lin, D.C., and Grossman, A.D. (1998) Identification and characterization of a bacterial chromosome partitioning site. Cell 92: 675-685.
40. Liu, D., Yumoto, H., Murakami, K., Hirota, K., Ono, T., Nagamune, H., etal. (2008) The essentiality and involvement of Streptococcus intermedius histone-like DNA-binding protein in bacterial viability and normal growth. Mol Microbiol 68: 1268-1282.
41. -ΔΔCT method. Methods 25: 402-408.
42. Livny, J., Yamaichi, Y., and Waldor, M.K. (2007) Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 189: 8693-8703.
43. Lutkenhaus, J. (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z-ring. Annu Rev Biochem 76: 539-562.
44. McClure, R., Balasubramanian, D., Sun, Y., Bobrovskyy, M., Sumby, P., Genco, C.A., etal. (2013) Computational analysis of bacterial RNA-Seq data. Nucleic Acids Res 41: e140-e140.
45. Martín-Galiano, A.J., and de la Campa, A.G. (2003) High-efficiency generation of antibiotic-resistant strains of Streptococcus pneumoniae by PCR and transformation. Antimicrob Agents Chemother 47: 1257-1261.
46. Martin, B., García, P., Castanié, M.P., and Claverys, J.P. (1995) The recA gene of Streptococcus pneumoniae is part of a competence-induced operon and controls lysogenic induction. Mol Microbiol 15: 367-379.
47. Mascarenhas, J., Soppa, J., Strunnikov, A.V., and Graumann, P.L. (2002) Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 21: 3108-3118.
48. Minnen, A., Attaiech, L., Thon, M., Gruber, S., and Veening, J.-W. (2011) SMC is recruited to oriC by ParB and promotes chromosome segregation in Streptococcus pneumoniae. Mol Microbiol 81: 676-688.
49. Moriya, S., Tsujikawa, E., Hassan, A.K., Asai, K., Kodama, T., and Ogasawara, N. (1998) A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol Microbiol 29: 179-187.
50. Morlot, C., Zapun, A., Dideberg, O., and Vernet, T. (2003) Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Mol Microbiol 50: 845-855.
51. Niki, H., Jaffé, A., Imamura, R., Ogura, T., and Hiraga, S. (1991) The new gene mukB codes for a 177kDa protein with coiled-coil domains involved in chromosome partitioning of E.coli. EMBO J 10: 183-193.
52. Nováková, L., Sasková, L., Pallová, P., Janecek, J., Novotná, J., Ulrych, A., etal. (2005) Characterization of a eukaryotic type serine/threonine protein kinase and protein phosphatase of Streptococcus pneumoniae and identification of kinase substrates. FEBS J 272: 1243-1254.
53. Pelve, E.A., Lindås, A.-C., Knöppel, A., Mira, A., and Bernander, R. (2012) Four chromosome replication origins in the archaeon Pyrobaculum calidifontis. Mol Microbiol 85: 986-995.
54. Pinho, M.G., Kjos, M., and Veening, J.-W. (2013) How to get (a)round: mechanisms controlling growth and division of coccoid bacteria. Nat Rev Microbiol 11: 601-614.
55. Possoz, C., Junier, I., and Espeli, O. (2012) Bacterial chromosome segregation. Front Biosci 17: 1020-1034.
56. Ptacin, J.L., Lee, S.F., Garner, E.C., Toro, E., Eckart, M., Comolli, L.R., etal. (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12: 791-798.
57. Reyes-Lamothe, R., Nicolas, E., and Sherratt, D.J. (2012) Chromosome replication and segregation in bacteria. Annu Rev Genet 46: 121-143.
58. Ryan, K.R., and Shapiro, L. (2003) Temporal and spatial regulation in prokaryotic cell cycle progression and development. Annu Rev Biochem 72: 367-394.
59. Shebelut, C.W., Guberman, J.M., Teeffelen, S., van Yakhnina, A.A., and Gitai, Z. (2010) Caulobacter chromosome segregation is an ordered multistep process. Proc Natl Acad Sci USA 107: 14194-14198.
60. Sherratt, D.J., Søballe, B., Barre, F.-X., Filipe, S., Lau, I., Massey, T., and Yates, J. (2004) Recombination and chromosome segregation. Philos Trans R Soc Lond B Biol Sci 359: 61-69.
61. Skarstad, K., Boye, E., and Steen, H.B. (1986) Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J 5: 1711-1717.
62. Spira, F., Dominguez-Escobar, J., Müller, N., and Wedlich-Söldner, R. (2012) Visualization of cortex organization and dynamics in microorganisms, using total internal reflection fluorescence microscopy. J Vis Exp 63: e3982.
63. Stouf, M., Meile, J.-C., and Cornet, F. (2013) FtsK actively segregates sister chromosomes in Escherichia coli. Proc Natl Acad Sci USA 110: 11157-11162.
64. Sullivan, N.L., Marquis, K.A., and Rudner, D.Z. (2009) Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137: 697-707.
65. Sun, Q., Yu, X.-C., and Margolin, W. (1998) Assembly of the FtsZ ring at the central division site in the absence of the chromosome. Mol Microbiol 29: 491-503.
66. Toro, E., and Shapiro, L. (2010) Bacterial chromosome organization and segregation. Cold Spring Harb Perspect Biol 2: a000349.
67. Tuske, S., Sarafianos, S.G., Wang, X., Hudson, B., Sineva, E., Mukhopadhyay, J., etal. (2005) Inhibition of bacterial RNA polymerase by streptolydigin: stabilization of a straight-bridge-helix active-center conformation. Cell 122: 541-552.
68. Usongo, V., Tanguay, C., Nolent, F., Bessong, J.E., and Drolet, M. (2013) Interplay between type 1A topoisomerases and gyrase in chromosome segregation in Escherichia coli. J Bacteriol 195: 1758-1768.
69. Vassylyev, D.G., Vassylyeva, M.N., Zhang, J., Palangat, M., Artsimovitch, I., and Landick, R. (2007) Structural basis for substrate loading in bacterial RNA polymerase. Nature 448: 163-168.
70. Vecchiarelli, A.G., Han, Y.-W., Tan, X., Mizuuchi, M., Ghirlando, R., Biertümpfel, C., etal. (2010) ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition. Mol Microbiol 78: 78-91.
71. Vecchiarelli, A.G., Mizuuchi, K., and Funnell, B.E. (2012) Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 86: 513-523.
72. Veiga, H., Jorge, A.M., and Pinho, M.G. (2011) Absence of nucleoid occlusion effector Noc impairs formation of orthogonal FtsZ rings during Staphylococcus aureus cell division. Mol Microbiol 80: 1366-1380.
73. Wang, X., and Sherratt, D.J. (2010) Independent segregation of the two arms of the Escherichia coli ori region requires neither RNA synthesis nor MreB dynamics. J Bacteriol 192: 6143-6153.
74. Wang, X., Llopis, P.M., and Rudner, D.Z. (2013) Organization and segregation of bacterial chromosomes. Nat Rev Genet 14: 191-203.
75. Woldringh, C.L. (2002) The role of co-transcriptional translation and protein translocation (transertion) in bacterial chromosome segregation. Mol Microbiol 45: 17-29.
76. Wu, L.J., and Errington, J. (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915-925.