Hypothesis: Local variations in the speed of individual DNA replication forks determine the phenotype of daughter cells
Main Article Content
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.
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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: 27 dec. 2024.
doi: https://doi.org/10.18103/mra.v5i12.1598.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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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.
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