Hypothesis: Local variations in the speed of individual DNA replication forks determine the phenotype of daughter cells

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Vic Norris Ina Koch Patrick Amar Francois Kepes Laurent Janniere

Abstract

How a cell coordinates its thousands of different constituents to achieve coherent – but different – phenotypes is far from fully understood. It is clear though that daughter cells with different phenotypes can be generated by the cell cycle, which comprises the events of chromosome replication, chromosome segregation and cell division. In line with this, recent experiments are consistent with an intimate relationship in bacteria between the speed of chromosome replication at a fork(s) and metabolism. The process of chromosome replication progressively changes the copy number of genes and sites in a linear order. This raises the possibility that speeding up or slowing down or even pausing replication for different times at different sites in the chromosome might be combined with various mechanisms leading to local cooperation (for example, the transcription of a gene leading to more transcription of that gene) and to global competition (for example, a gene having to compete with all the other genes for the transcriptional apparatus). If so, such replication-phenotype coupling could produce different patterns of gene expression and metabolic activity. Indeed, replication-phenotype coupling may constitute a powerful and fundamental way of generating coherent phenotypes, that is, phenotypes in which the cell's constituents perform compatible functions (rather than, for example, trying to maintain growth and to shut down growth simultaneously). In this hypothesis, such coupling would involve the dynamics of the spatially extended assemblies of molecules and macromolecules termed 'hyperstructures'. As a prelude to testing this hypothesis, we discuss some of the parameters that will need to be explored by bench experimentation and computer simulation.

Article Details

How to Cite
NORRIS, Vic et al. Hypothesis: Local variations in the speed of individual DNA replication forks determine the phenotype of daughter cells. Medical Research Archives, [S.l.], v. 5, n. 12, dec. 2017. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/1598>. Date accessed: 28 mar. 2024. doi: https://doi.org/10.18103/mra.v5i12.1598.
Section
Research Articles

References

References
1. Kauffman S. The origins of order. Oxford: Oxford University Press; 1993.
2. Norris V, Gascuel P, Guespin-Michel J, Ripoll C, Saier MH, Jr. Metabolite-induced metabolons: the activation of transporter-enzyme complexes by substrate binding. Mol Microbiol. 1999;31(5):1592-5.
3. Norris V, Blaauwen TD, Doi RH, Harshey RM, Janniere L, Jimenez-Sanchez A, et al. Toward a Hyperstructure Taxonomy. Annu Rev Microbiol. 2007;61:309-29.
4. Norris V, Menu-Bouaouiche L, Becu J-M, Legendre R, Norman R, Rosenzweig JA. Hyperstructure interactions influence the virulence of the Type 3 secretion system in yersiniae and other bacteria. Appl Microbiol Biotechnol. 2012;96(1):23-36.
5. Saier MH, Jr. Microcompartments and protein machines in prokaryotes. J Mol Microbiol Biotechnol. 2013;23(4-5):243-69.
6. Norris V, Verrier C, Feuilloley M. Hybolites Revisited. Recent Pat Antiinfect Drug Discov. 2016;11(1):16-31.
7. Booth IR. Stress and the single cell: intrapopulation diversity is a mechanism to ensure survival upon exposure to stress. International Journal of Food Microbiology. 2002;78:19-30.
8. Avery SV. Microbial cell individuality and the underlying sources of heterogeneity. Nat Rev Microbiol. 2006;4(8):577-87.
9. Smits WK, Kuipers OP, Veening JW. Phenotypic variation in bacteria: the role of feedback regulation. Nat Rev Microbiol. 2006;4(4):259-71.
10. Bergmiller T, Andersson AMC, Tomasek K, Balleza E, Kiviet DJ, Hauschild R, et al. Biased partitioning of the multidrug efflux pump AcrAB-TolC underlies long-lived phenotypic heterogeneity. Science. 2017;356(6335):311-5.
11. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science. 2004;305(5690):1622-5.
12. Wang P, Robert L, Pelletier J, Dang WL, Taddei F, Wright A, et al. Robust growth of Escherichia coli. Curr Biol. 2010;20(12):1099-103.
13. Gangwe Nana G, Gibouin D, Lefebvre F, Delaune A, Jannière L, Ripoll C, et al., editors. Intracellular and population heterogeneity in Bacillus subtilis revealed by Secondary Ion Mass Spectrometry. Modelling complex biological systems in the context of genomics; 2012; Evry, France: EDP Sciences.
14. Norris V. Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane-domain formation. Mol Microbiol. 1995;16(6):1051-7.
15. Norris V, Demarty M, Raine D, Cabin-Flaman A, Le Sceller L. Hypothesis: hyperstructures regulate initiation in Escherichia coli and other bacteria. Biochimie. 2002;84:341-7.
16. Rocha EP, Fralick J, Vediyappan G, Danchin A, Norris V. A strand-specific model for chromosome segregation in bacteria. Mol Microbiol. 2003;49(4):895-903.
17. Breier AM, Weier HU, Cozzarelli NR. Independence of replisomes in Escherichia coli chromosomal replication. Proceedings of the National Academy of Science USA. 2005;102:3942-7.
18. Graham JE, Marians KJ, Kowalczykowski SC. Independent and Stochastic Action of DNA Polymerases in the Replisome. Cell. 2017;169(7):1201-13 e17.
19. Guijo MI, Patte J, del Mar Campos M, Louarn JM, Rebollo JE. Localized remodeling of the Escherichia coli chromosome: the patchwork of segments refractory and tolerant to inversion near the replication terminus. Genetics. 2001;157(4):1413-23.
20. Autret S, Levine A, Vannier F, Fujita Y, Seror SJ. The replication checkpoint control in Bacillus subtilis: identification of a novel RTP-binding sequence essential for the replication fork arrest after induction of the stringent response. Mol Microbiol. 1999;31(6):1665-79.
21. Mulugu S, Potnis A, Shamsuzzaman, Taylor J, Alexander K, Bastia D. Mechanism of termination of DNA replication of Escherichia coli involves helicase-contrahelicase interaction. Proc Natl Acad Sci U S A. 2001;98(17):9569-74.
22. Denapoli J, Tehranchi AK, Wang JD. Dose-dependent reduction of replication elongation rate by (p)ppGpp in Escherichia coli and Bacillus subtilis. Mol Microbiol. 2013;88(1):93-104.
23. Maduike NZ, Tehranchi AK, Wang JD, Kreuzer KN. Replication of the Escherichia coli chromosome in RNase HI-deficient cells: multiple initiation regions and fork dynamics. Mol Microbiol. 2014;91(1):39-56.
24. Tan KW, Pham TM, Furukohri A, Maki H, Akiyama MT. Recombinase and translesion DNA polymerase decrease the speed of replication fork progression during the DNA damage response in Escherichia coli cells. Nucleic Acids Res. 2015;43(3):1714-25.
25. Lieder S, Jahn M, Koepff J, Muller S, Takors R. Environmental stress speeds up DNA replication in Pseudomonas putida in chemostat cultivations. Biotechnol J. 2016;11(1):155-63.
26. Helmstetter CE. Timing of synthetic activities in the cell cycle. In: Neidhardt FC, Curtiss III R, Ingraham JL, Lin ECC, Low KB, Magasanik B, et al., editors. Escherichia coli and Salmonella. Washington D.C.: American Society for Microbiology; 1991. p. 1594-605.
27. Michelsen O, Teixeira de Mattos MJ, Jensen PR, Hansen FG. Precise determinations of C and D periods by flow cytometry in Escherichia coli K-12 and B/r. Microbiology. 2003;149:1001-10.
28. Maciag M, Nowicki D, Janniere L, Szalewska-Palasz A, Wegrzyn G. Genetic response to metabolic fluctuations: correlation between central carbon metabolism and DNA replication in Escherichia coli. Microb Cell Fact. 2011;10:19.
29. Noirot-Gros MF, Dervyn E, Wu LJ, Mervelet P, Errington J, Ehrlich SD, et al. An expanded view of bacterial DNA replication. Proceedings of the National Academy of Science USA. 2002;99:8342-7.
30. Stein A, Firshein W. Probable identification of a membrane-associated repressor of Bacillus subtilis DNA replication as the E2 subunit of the pyruvate dehydrogenase complex. Journal of Bacteriology. 2000;182:2119-24.
31. Rannou O, Le Chatelier E, Larson MA, Nouri H, Dalmais B, Laughton C, et al. Functional interplay of DnaE polymerase, DnaG primase and DnaC helicase within a ternary complex, and primase to polymerase hand-off during lagging strand DNA replication in Bacillus subtilis. Nucleic Acids Res. 2013;41(10):5303-20.
32. Paschalis V, Le Chatelier E, Green M, Kepes F, Soultanas P, Janniere L. Interactions of the Bacillus subtilis DnaE polymerase with replisomal proteins modulate its activity and fidelity. Open Biol. 2017;7(9).
33. Janniere L, Canceill D, Suski C, Kanga S, Dalmais B, Lestini R, et al. Genetic evidence for a link between glycolysis and DNA replication. PLoS One. 2007;2(5):e447.
34. Sobetzko P, Travers A, Muskhelishvili G. Gene order and chromosome dynamics coordinate spatiotemporal gene expression during the bacterial growth cycle. Proc Natl Acad Sci U S A. 2012;109(2):E42-50.
35. Kepes F. Periodic epi-organization of the yeast genome revealed by the distribution of promoter sites. J Mol Biol. 2003;329(5):859-65.
36. Kepes F. Periodic transcriptional organization of the E.coli genome. J Mol Biol. 2004;340(5):957-64.
37. Gerganova V, Berger M, Zaldastanishvili E, Sobetzko P, Lafon C, Mourez M, et al. Chromosomal position shift of a regulatory gene alters the bacterial phenotype. Nucleic Acids Res. 2015;43(17):8215-26.
38. Vora T, Hottes AK, Tavazoie S. Protein occupancy landscape of a bacterial genome. Mol Cell. 2009;35(2):247-53.
39. Kuhlman TE, Cox EC. Gene location and DNA density determine transcription factor distributions in Escherichia coli. Mol Syst Biol. 2012;8:610.
40. Sousa C, de Lorenzo V, Cebolla A. Modulation of gene expression through chromosomal positioning in Escherichia coli. Microbiology. 1997;143 ( Pt 6):2071-8.
41. Bryant JA, Sellars LE, Busby SJ, Lee DJ. Chromosome position effects on gene expression in Escherichia coli K-12. Nucleic Acids Res. 2014;42(18):11383-92.
42. Brambilla E, Sclavi B. Gene regulation by H-NS as a function of growth conditions depends on chromosomal position in Escherichia coli. G3 (Bethesda). 2015;5(4):605-14.
43. Narula J, Kuchina A, Lee DY, Fujita M, Suel GM, Igoshin OA. Chromosomal Arrangement of Phosphorelay Genes Couples Sporulation and DNA Replication. Cell. 2015;162(2):328-37.
44. Miller OL, Jr., Hamkalo BA, Thomas CA, Jr. Visualization of bacterial genes in action. Science. 1970;169(943):392-5.
45. French SL, Miller OL, Jr. Transcription mapping of the Escherichia coli chromosome by electron microscopy. J Bacteriol. 1989;171(8):4207-16.
46. Burmann BM, Schweimer K, Luo X, Wahl MC, Stitt BL, Gottesman ME, et al. A NusE:NusG complex links transcription and translation. Science. 2010;328(5977):501-4.
47. Bakshi S, Choi H, Weisshaar JC. The spatial biology of transcription and translation in rapidly growing Escherichia coli. Front Microbiol. 2015;6:636.
48. Elgamal S, Artsimovitch I, Ibba M. Maintenance of Transcription-Translation Coupling by Elongation Factor P. MBio. 2016;7(5).
49. Kohler R, Mooney RA, Mills DJ, Landick R, Cramer P. Architecture of a transcribing-translating expressome. Science. 2017;356(6334):194-7.
50. Llopis PM, Jackson AF, Sliusarenko O, Surovtsev I, Heinritz J, Emonet T, et al. Spatial organization of the flow of genetic information in bacteria. Nature. 2010;466(7302):77-81.
51. Shieh YW, Minguez P, Bork P, Auburger JJ, Guilbride DL, Kramer G, et al. Operon structure and cotranslational subunit association direct protein assembly in bacteria. Science. 2015;350(6261):678-80.
52. Meyer P, Cecchi G, Stolovitzky G. Spatial localization of the first and last enzymes effectively connects active metabolic pathways in bacteria. BMC Syst Biol. 2014;8(1):131.
53. Lemon KP, Grossman AD. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science. 1998;282(5393):1516-9.
54. Migocki MD, Lewis PJ, Wake RG, Harry EJ. The midcell replication factory in Bacillus subtilis is highly mobile: implications for coordinating chromosome replication with other cell cycle events. Molecular Microbiology. 2004;54:452-63.
55. Sanchez-Romero MA, Molina F, Jimenez-Sanchez A. Organization of ribonucleoside diphosphate reductase during multifork chromosome replication in Escherichia coli. Microbiology. 2011;157(Pt 8):2220-5.
56. Rocha EP. The organization of the bacterial genome. Annu Rev Genet. 2008;42:211-33.
57. Cabrera JE, Jin DJ. The distribution of RNA polymerase in Escherichia coli is dynamic and sensitive to environmental cues. Molecular Microbiology. 2003;50:1493-505.
58. Jin DJ, Mata Martin C, Sun Z, Cagliero C, Zhou YN. Nucleolus-like compartmentalization of the transcription machinery in fast-growing bacterial cells. Crit Rev Biochem Mol Biol. 2017;52(1):96-106.
59. Srivatsan A, Tehranchi A, MacAlpine DM, Wang JD. Co-orientation of replication and transcription preserves genome integrity. PLoS Genet. 2010;6(1):e1000810.
60. Leonard AC, Grimwade JE. Building a bacterial orisome: emergence of new regulatory features for replication origin unwinding. Molecular Microbiology. 2005;55:978-85.
61. Messer W, Weigel C. DnaA initiator--also a transcription factor. Molecular Microbiology. 1997;24:1-6.
62. Hansen FG, Christensen BB, Atlung T. The initiator titration model: computer simulation of chromosome and minichromosome control. Research in Microbiology. 1991;142:161-7.
63. Dame RT, Wyman C, Goosen N. H-NS mediated compaction of DNA visualised by atomic force microscopy. Nucleic Acids Research. 2000;28:3504-10.
64. Oshima T, Ishikawa S, Kurokawa K, Aiba H, Ogasawara N. Escherichia coli histone-like protein H-NS preferentially binds to horizontally acquired DNA in association with RNA polymerase. DNA Res. 2006;13(4):141-53.
65. Pul U, Wurm R, Wagner R. The Role of LRP and H-NS in Transcription Regulation: Involvement of Synergism, Allostery and Macromolecular Crowding. J Mol Biol. 2007;366(3):900-15.
66. Müller-Hill B. The function of auxiliary operators. Molecular Microbiology. 1998;29:13-8.
67. von Hippel PH, Berg OG. On the specificity of DNA-protein interactions. Proc Natl Acad Sci U S A. 1986;83(6):1608-12.
68. Andersen PA, Griffiths AA, Duggin IG, Wake RG. Functional specificity of the replication fork-arrest complexes of Bacillus subtilis and Escherichia coli: significant specificity for Tus-Ter functioning in E. coli. Mol Microbiol. 2000;36(6):1327-35.
69. Valjavec-Gratian M, Henderson TA, Hill TM. Tus-mediated arrest of DNA replication in Escherichia coli is modulated by DNA supercoiling. Mol Microbiol. 2005;58(3):758-73.
70. Bidnenko V, Lestini R, Michel B. The Escherichia coli UvrD helicase is essential for Tus removal during recombination-dependent replication restart from Ter sites. Mol Microbiol. 2006;62(2):382-96.
71. Payne BT, van Knippenberg IC, Bell H, Filipe SR, Sherratt DJ, McGlynn P. Replication fork blockage by transcription factor-DNA complexes in Escherichia coli. Nucleic Acids Res. 2006;34(18):5194-202.
72. Cabin-Flaman A, Monnier AF, Coffinier Y, Audinot JN, Gibouin D, Wirtz T, et al. Combed Single DNA Molecules Imaged by Secondary Ion Mass Spectrometry. Anal Chem. 2011;83(18):6940-7.
73. Cabin-Flaman A, Monnier AF, Coffinier Y, Audinot JN, Gibouin D, Wirtz T, et al. Combining combing and secondary ion mass spectrometry to study DNA on chips using (13)C and (15)N labeling. F1000Res. 2016;5:1437.
74. Le Sceller L, Ripoll C, Demarty M, Cabin-Flaman A, Nyström T, Saier Jnr. M, et al. Modelling bacterial hyperstructures with cellular automata. Interjournal of Complex Systems. 2000;Paper 366:http://www.lri.fr/~pa/Hsim/InterJournal.pdf.
75. Ballet P, Zemirline A, Marcé L. The BioDyn language and simulator. Application to an immune response and E. coli and phage interaction. Journal of Biological Physics and Chemistry. 2004;4:93-101.
76. Soula H, Robardet C, Perrin F, Gripon S, Beslon G, Gandrillon O. Modeling the emergence of multi-protein dynamic structures by principles of self-organization through the use of 3DSpi, a Multi-Agent-based Software. Biomed Central Bioinformatics. 2005;6:228.
77. Amar P, Legent G, Thellier M, Ripoll C, Bernot G, Nystrom T, et al. A stochastic automaton shows how enzyme assemblies may contribute to metabolic efficiency. BMC Syst Biol. 2008;2:27.
78. Koch I, Nothen J, Schleiff E. Modeling the Metabolism of Arabidopsis thaliana: Application of Network Decomposition and Network Reduction in the Context of Petri Nets. Front Genet. 2017;8:85.
79. Norris V, den Blaauwen T, Cabin-Flaman A, Doi RH, Harshey R, Janniere L, et al. Functional taxonomy of bacterial hyperstructures. Microbiol Mol Biol Rev. 2007;71(1):230-53.
80. Norris V. Why do bacteria divide? Front Microbiol. 2015;6:322.
81. Norris V, Madsen MS. Autocatalytic gene expression occurs via transertion and membrane domain formation and underlies differentiation in bacteria: a model. J Mol Biol. 1995;253(5):739-48.
82. Teleman AA, Graumann PL, Lin DC, Grossman AD, Losick R. Chromosome arrangement within a bacterium. Current Biology. 1998;8:1102–9.
83. Niki H, Yamaichi Y, Hiraga S. Dynamic organization of chromosomal DNA in Escherichia coli. Genes and Development. 2000;14:212–23.
84. Viollier PH, Thanbichler M, McGrath PT, West L, Meewan M, McAdams HH, et al. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proceedings of the National Academy of Science USA. 2004;101:9257-62.
85. Junier I, Martin O, Kepes F. Spatial and topological organization of DNA chains induced by gene co-localization. PLoS Comput Biol. 2010;6(2):e1000678.
86. Kepes F, Jester BC, Lepage T, Rafiei N, Rosu B, Junier I. The layout of a bacterial genome. FEBS Lett. 2012.