Recollections of a Helmstetter Disciple
Abstract
:1. Introduction
2. Making E. coli Minichromosomes and Cell Cycle Analysis
3. Searching for Cell Cycle-Specificity in Plasmid Systems
4. A Sidestep into the Role of DNA Supercoiling in Minichromosome Regulation
5. Studying the Non-Random Segregation of Minichromosomes
6. Discussion
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Marsh, R.C.; Worcel, A. A DNA fragment containing the origin of replication of the Escherichia coli chromosome. Proc. Natl. Acad. Sci. USA 1977, 74, 2720–2724. [Google Scholar] [CrossRef] [PubMed]
- von Meyenburg, K.; Hansen, F.G.; Nielsen, L.D.; Jørgensen, P. Origin of replication, oriC, of the Escherichia coli chromosome: Mapping of genes relative to R.EcoRI cleavage sites in the oriC region. Mol. Gen. Genet. 1977, 158, 101–109. [Google Scholar] [CrossRef] [PubMed]
- Timmis, K.N.; Cabello, F.; Cohen, S.N. Cloning and characterization of EcoRI and HindIII restriction endonuclease-generated fragments of antibiotic resistance plasmids R6-5 and R6. Mol. Gen. Genet. 1978, 162, 121–137. [Google Scholar] [CrossRef]
- Helmstetter, C.E. A ten-year search for synchronous cells: Obstacles, solutions, and practical applications. Front. Microbiol. 2015, 6, 238. [Google Scholar] [CrossRef]
- Cooper, S.; Helmstetter, C.E. Chromosome replication and the division cycle of Escherichia coli B/r. J. Mol. Biol. 1968, 31, 519–540. [Google Scholar] [CrossRef]
- Helmstetter, C.; Cooper, S.; Pierucci, O.; Revelas, E. On the bacterial life sequence. Cold Spring Harb. Symp. Quant. Biol. 1968, 33, 809–822. [Google Scholar] [CrossRef] [PubMed]
- Yasuda, S.; Hirota, Y. Cloning and mapping of the replication origin of Escherichia coli. Proc. Natl. Acad. Sci. USA 1977, 74, 5458–5462. [Google Scholar] [CrossRef]
- Meijer, M.; Beck, E.; Hansen, F.G.; Bergmans, H.E.; Messer, W.; von Meyenburg, K.; Schaller, H. Nucleotide sequence of the origin of replication of the Escherichia coli K-12 chromosome. Proc. Natl. Acad. Sci. USA 1979, 76, 580–584. [Google Scholar] [CrossRef]
- Fuller, R.S.; Kaguni, J.M.; Kornberg, A. Enzymatic replication of the origin of the Escherichia coli chromosome. Proc. Natl. Acad. Sci. USA 1981, 78, 7370–7374. [Google Scholar] [CrossRef]
- Leonard, A.C.; Helmstetter, C.E. Cell cycle-specific replication of Escherichia coli minichromosomes. Proc. Natl. Acad. Sci. USA 1986, 83, 5101–5105. [Google Scholar] [CrossRef]
- Helmstetter, C.E.; Leonard, A.C. Coordinate initiation of chromosome and minichromosome replication in Escherichia coli. J. Bacteriol. 1987, 169, 3489–3494. [Google Scholar] [CrossRef] [PubMed]
- Abeles, A.L.; Snyder, K.M.; Chattoraj, D.K. P1 plasmid replication: Replicon structure. J. Mol. Biol. 1984, 173, 307–324. [Google Scholar] [CrossRef] [PubMed]
- Vocke, C.; Bastia, D. Primary structure of the essential replicon of the plasmid pSC101. Proc. Natl. Acad. Sci. USA 1983, 80, 6557–6561. [Google Scholar] [CrossRef]
- Masai, H.; Arai, K. RepA and DnaA proteins are required for initiation of R1 plasmid replication in vitro and interact with the oriR sequence. Proc. Natl. Acad. Sci. USA 1987, 84, 4781–4785. [Google Scholar] [CrossRef]
- Murakami, Y.; Ohmori, H.; Yura, T.; Nagata, T. Requirement of the Escherichia coli dnaA gene function for ori-2-dependent mini-F plasmid replication. J. Bacteriol. 1987, 169, 1724–1730. [Google Scholar] [CrossRef]
- Leonard, A.C.; Helmstetter, C.E. Replication patterns of multiple plasmids coexisting in Escherichia coli. J. Bacteriol. 1988, 170, 1380–1383. [Google Scholar] [CrossRef] [PubMed]
- Morrison, P.D.; Chattoraj, D.K. Replication of a unit-copy plasmid F in the bacterial cell cycle: A replication rate function analysis. Plasmid 2004, 52, 13–30. [Google Scholar] [CrossRef]
- Bogan, J.A.; Grimwade, J.E.; Thornton, M.; Zhou, P.; Denning, G.D.; Helmstetter, C.E. P1 and NR1 plasmid replication during the cell cycle of Escherichia coli. Plasmid 2001, 45, 200–208. [Google Scholar] [CrossRef]
- Keasling, J.D.; Palsson, B.O.; Cooper, S. Replication of the R6K plasmid during the Escherichia coli cell cycle. J. Bacteriol. 1992, 174, 1060–1062. [Google Scholar] [CrossRef]
- Keasling, J.D.; Palsson, B.O.; Cooper, S. Replication of prophage P1 is cell-cycle specific. J. Bacteriol. 1992, 174, 4457–4462. [Google Scholar] [CrossRef]
- Keasling, J.D.; Palsson, B.O.; Cooper, S. Cell-cycle-specific F plasmid replication: Regulation by cell size control of initiation. J. Bacteriol. 1991, 173, 2673–2680. [Google Scholar] [CrossRef] [PubMed]
- Keasling, J.D.; Palsson, B.O.; Cooper, S. Replication of mini-F plasmids during the bacterial division cycle. Res. Microbiol. 1992, 143, 541–548. [Google Scholar] [CrossRef] [PubMed]
- Mukhopadhyay, G.; Carr, K.M.; Kaguni, J.M.; Chattoraj, D.K. Open-complex formation by the host initiator, DnaA, at the origin of P1 plasmid replication. EMBO J. 1993, 12, 4547–4554. [Google Scholar] [CrossRef] [PubMed]
- Wu, F.; Levchenko, I.; Filutowicz, M. Binding of DnaA protein to a replication enhancer counteracts the inhibition of plasmid R6K gamma origin replication mediated by elevated levels of R6K pi protein. J. Bacteriol. 1994, 176, 6795–6801. [Google Scholar] [CrossRef] [PubMed]
- Drlica, K. Bacterial topoisomerases and the control of DNA supercoiling. Trends Genet. 1990, 6, 433–437. [Google Scholar] [CrossRef] [PubMed]
- Muskhelishvili, G.; Travers, A. The regulatory role of DNA supercoiling in nucleoprotein complex assembly and genetic activity. Biophys. Rev. 2016, 8, 5–22. [Google Scholar] [CrossRef] [PubMed]
- Leonard, A.C.; Whitford, W.G.; Helmstetter, C.E. Involvement of DNA superhelicity in minichromosome maintenance in Escherichia coli. J. Bacteriol. 1985, 161, 687–695. [Google Scholar] [CrossRef]
- von Freiesleben, U.; Rasmussen, K.V. The level of supercoiling affects the regulation of DNA replication in Escherichia coli. Res. Microbiol. 1992, 143, 655–663. [Google Scholar] [CrossRef]
- Skarstad, K.; Baker, T.A.; Kornberg, A. Strand separation required for initiation of replication at the chromosomal origin of E.coli is facilitated by a distant RNA--DNA hybrid. EMBO J. 1990, 9, 2341–2348. [Google Scholar] [CrossRef]
- Baker, T.A.; Kornberg, A. Transcriptional activation of initiation of replication from the E. coli chromosomal origin: An RNA-DNA hybrid near oriC. Cell 1988, 55, 113–123. [Google Scholar] [CrossRef]
- El Houdaigui, B.; Forquet, R.; Hindré, T.; Schneider, D.; Nasser, W.; Reverchon, S.; Meyer, S. Bacterial genome architecture shapes global transcriptional regulation by DNA supercoiling. Nucleic Acids Res. 2019, 47, 5648–5657. [Google Scholar] [CrossRef] [PubMed]
- Kraemer, J.A.; Sanderlin, A.G.; Laub, M.T. The Stringent Response Inhibits DNA Replication Initiation in E. coli by Modulating Supercoiling of oriC. mBio 2019, 10, e01330-19. [Google Scholar] [CrossRef] [PubMed]
- Dorman, C.J. DNA supercoiling and transcription in bacteria: A two-way street. BMC Mol. Cell Biol. 2019, 20, 26. [Google Scholar] [CrossRef] [PubMed]
- Pierucci, O.; Zuchowski, C. Non-random segregation of DNA strands in Escherichia coli B-r. J. Mol. Biol. 1973, 80, 477–503. [Google Scholar] [CrossRef]
- Pierucci, O.; Helmstetter, C.E. Chromosome segregation in Escherichia coli B/r at various growth rates. J. Bacteriol. 1976, 128, 708–716. [Google Scholar] [CrossRef]
- Cooper, S.; Weinberger, M. Medium-dependent variation of deoxyribonucleic acid segregation in Escherichia coli. J. Bacteriol. 1977, 130, 118–127. [Google Scholar] [CrossRef]
- Helmstetter, C.E.; Leonard, A.C. Mechanism for chromosome and minichromosome segregation in Escherichia coli. J. Mol. Biol. 1987, 197, 195–204. [Google Scholar] [CrossRef]
- Helmstetter, C.E.; Leonard, A.C. Involvement of cell shape in the replication and segregation of chromosomes in Escherichia coli. Res. Microbiol. 1990, 141, 30–39. [Google Scholar] [CrossRef]
- Schurr, T.; Grover, N.B. Analysis of a model for minichromosome segregation in Escherichia coli. J. Theor. Biol. 1990, 146, 395–406. [Google Scholar] [CrossRef]
- Hendrickson, W.G.; Kusano, T.; Yamaki, H.; Balakrishnan, R.; King, M.; Murchie, J.; Schaechter, M. Binding of the origin of replication of Escherichia coli to the outer membrane. Cell 1982, 30, 915–923. [Google Scholar] [CrossRef]
- Landoulsi, A.; Malki, A.; Kern, R.; Kohiyama, M.; Hughes, P. The E. coli cell surface specifically prevents the initiation of DNA replication at oriC on hemimethylated DNA templates. Cell 1990, 63, 1053–1060. [Google Scholar] [CrossRef] [PubMed]
- Boeneman, K.; Crooke, E. Chromosomal replication and the cell membrane. Curr. Opin. Microbiol. 2005, 8, 143–148. [Google Scholar] [CrossRef] [PubMed]
- Saxena, R.; Fingland, N.; Patil, D.; Sharma, A.K.; Crooke, E. Crosstalk between DnaA protein, the initiator of Escherichia coli chromosomal replication, and acidic phospholipids present in bacterial membranes. Int. J. Mol. Sci 2013, 14, 8517–8537. [Google Scholar] [CrossRef] [PubMed]
- Regev, T.; Meyers, N.; Zarivach, R.; Fishov, I. Association of the chromosome replication initiator DnaA with the Escherichia coli inner membrane in vivo: Quantity and mode of binding. PLoS ONE 2012, 7, e36441. [Google Scholar] [CrossRef]
- Lee, S.; Wu, L.J.; Errington, J. Microfluidic time-lapse analysis and reevaluation of the Bacillus subtilis cell cycle. Microbiologyopen 2019, 8, e876. [Google Scholar] [CrossRef]
- Zhang, Q.; Zhang, Z.; Shi, H. Cell Size Is Coordinated with Cell Cycle by Regulating Initiator Protein DnaA in E. coli. Biophys. J. 2020, 119, 2537–2557. [Google Scholar] [CrossRef]
- Kar, P.; Tiruvadi-Krishnan, S.; Männik, J.; Männik, J.; Amir, A. Using conditional independence tests to elucidate causal links in cell cycle regulation in Escherichia coli. Proc. Natl. Acad. Sci. USA 2023, 120, e2214796120. [Google Scholar] [CrossRef]
- Le Treut, G.; Si, F.; Li, D.; Jun, S. Quantitative Examination of Five Stochastic Cell-Cycle and Cell-Size Control Models for Escherichia coli and Bacillus subtilis. Front. Microbiol. 2021, 12, 721899. [Google Scholar] [CrossRef]
- Tiruvadi-Krishnan, S.; Männik, J.; Kar, P.; Lin, J.; Amir, A.; Männik, J. Coupling between DNA replication, segregation, and the onset of constriction in Escherichia coli. Cell Rep. 2022, 38, 110539. [Google Scholar] [CrossRef]
- Wallden, M.; Fange, D.; Lundius, E.G.; Baltekin, Ö.; Elf, J. The Synchronization of Replication and Division Cycles in Individual E. coli Cells. Cell 2016, 166, 729–739. [Google Scholar] [CrossRef]
- Taheri-Araghi, S.; Bradde, S.; Sauls, J.T.; Hill, N.S.; Levin, P.A.; Paulsson, J.; Vergassola, M.; Jun, S. Cell-size control and homeostasis in bacteria. Curr. Biol. 2015, 25, 385–391. [Google Scholar] [CrossRef] [PubMed]
- Witz, G.; van Nimwegen, E.; Julou, T. Initiation of chromosome replication controls both division and replication cycles in E. coli through a double-adder mechanism. Elife 2019, 8, e48063. [Google Scholar] [CrossRef] [PubMed]
- Leonard, A.C.; Grimwade, J.E. Regulation of DnaA assembly and activity: Taking directions from the genome. Annu Rev. Microbiol. 2011, 65, 19–35. [Google Scholar] [CrossRef] [PubMed]
- Hansen, F.G.; Christensen, B.B.; Atlung, T. The initiator titration model: Computer simulation of chromosome and minichromosome control. Res. Microbiol. 1991, 142, 161–167. [Google Scholar] [CrossRef] [PubMed]
- Berger, M.; Wolde, P.R.T. Robust replication initiation from coupled homeostatic mechanisms. Nat. Commun. 2022, 13, 6556. [Google Scholar] [CrossRef] [PubMed]
- Zheng, H.; Bai, Y.; Jiang, M.; Tokuyasu, T.A.; Huang, X.; Zhong, F.; Wu, Y.; Fu, X.; Kleckner, N.; Hwa, T.; et al. General quantitative relations linking cell growth and the cell cycle in Escherichia coli. Nat. Microbiol. 2020, 5, 995–1001. [Google Scholar] [CrossRef]
- Pritchard, R.H.; Barth, P.T.; Collins, J. Control of DNA synthesis in bacteria. Symp. Soc. Gen. Microbiol. 1969, 19, 263–297. [Google Scholar]
- diCenzo, G.C.; Finan, T.M. The divided bacterial genome: Structure, function, and evolution. Microbiol. Mol. Biol Rev. 2017, 81, 9–17. [Google Scholar] [CrossRef]
- Fournes, F.; Val, M.E.; Skovgaard, O.; Mazel, D. Replicate Once Per Cell Cycle: Replication Control of Secondary Chromosomes. Front. Microbiol. 2018, 9, 1833. [Google Scholar] [CrossRef]
- Ramachandran, R.; Jha, J.; Paulsson, J.; Chattoraj, D. Random versus Cell Cycle-Regulated Replication Initiation in Bacteria: Insights from Studying Vibrio cholerae Chromosome 2. Microbiol. Mol. Biol. Rev. 2017, 81, e00033-16. [Google Scholar] [CrossRef]
- Espinosa, E.; Barre, F.X.; Galli, E. Coordination between replication, segregation and cell division in multi-chromosomal bacteria: Lessons from Vibrio cholerae. Int. Microbiol. 2017, 20, 121–129. [Google Scholar] [PubMed]
- Venkova-Canova, T.; Chattoraj, D.K. Transition from a plasmid to a chromosomal mode of replication entails additional regulators. Proc. Natl. Acad. Sci. USA 2011, 108, 6199–6204. [Google Scholar] [CrossRef] [PubMed]
- de Lemos Martins, F.; Fournes, F.; Mazzuoli, M.-V.; Mazel, D.; Val, M.-E. Vibrio cholerae chromosome 2 copy number is controlled by the methylation-independent binding of its monomeric initiator to the chromosome 1 crtS site. Nucleic Acids Res. 2018, 46, 10145–10156. [Google Scholar] [CrossRef] [PubMed]
- Fournes, F.; Niault, T.; Czarnecki, J.; Tissier-Visconti, A.; Mazel, D.; Val, M.-E. The coordinated replication of Vibrio cholerae’s two chromosomes required the acquisition of a unique domain by the RctB initiator. Nucleic Acids Res. 2021, 49, 11119–11133. [Google Scholar] [CrossRef] [PubMed]
- Muskhelishvili, G.; Sobetzko, P.; Travers, A. Spatiotemporal Coupling of DNA Supercoiling and Genomic Sequence Organization-A Timing Chain for the Bacterial Growth Cycle. Biomolecules 2022, 12, 831. [Google Scholar] [CrossRef] [PubMed]
- Verma, S.C.; Qian, Z.; Adhya, S.L. Architecture of the Escherichia coli nucleoid. PLoS Genet. 2019, 15, e1008456. [Google Scholar] [CrossRef]
- Mäkelä, J.; Uphoff, S.; Sherratt, D.J. Nonrandom segregation of sister chromosomes by Escherichia coli MukBEF. Proc. Natl. Acad. Sci. USA 2021, 118, e2022078118. [Google Scholar] [CrossRef]
- White, M.A.; Eykelenboom, J.K.; Lopez-Vernaza, M.A.; Wilson, E.; Leach, D.R. Non-random segregation of sister chromosomes in Escherichia coli. Nature 2008, 455, 1248–1250. [Google Scholar] [CrossRef]
- Lopez-Vernaza, M.A.; Leach, D.R. Symmetries and asymmetries associated with non-random segregation of sister DNA strands in Escherichia coli. Semin Cell Dev. Biol. 2013, 24, 610–617. [Google Scholar] [CrossRef]
- Mäkelä, J.; Sherratt, D. SMC complexes organize the bacterial chromosome by lengthwise compaction. Curr. Genet. 2020, 66, 895–899. [Google Scholar] [CrossRef]
- Bürmann, F.; Lee, B.G.; Than, T.; Sinn, L.; O’Reilly, F.J.; Yatskevich, S.; Rappsilber, J.; Hu, B.; Nasmyth, K.; Löwe, J. A folded conformation of MukBEF and cohesin. Nat. Struct. Mol. Biol. 2019, 26, 227–236. [Google Scholar] [CrossRef] [PubMed]
- Nolivos, S.; Upton, A.L.; Badrinarayanan, A.; Müller, J.; Zawadzka, K.; Wiktor, J.; Gill, A.; Arciszewska, L.; Nicolas, E.; Sherratt, D. MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation. Nat. Commun. 2016, 7, 10466. [Google Scholar] [CrossRef] [PubMed]
- Mäkelä, J.; Sherratt, D.J. Organization of the Escherichia coli Chromosome by a MukBEF Axial Core. Mol. Cell 2020, 78, 250–260.e5. [Google Scholar] [CrossRef] [PubMed]
- Japaridze, A.; van Wee, R.; Gogou, C.; Kerssemakers, J.W.J.; van den Berg, D.F.; Dekker, C. MukBEF-dependent chromosomal organization in widened Escherichia coli. Front. Microbiol. 2023, 14, 1107093. [Google Scholar] [CrossRef] [PubMed]
- Hofmann, A.; Mäkelä, J.; Sherratt, D.J.; Heermann, D.; Murray, S.M. Self-organised segregation of bacterial chromosomal origins. Elife 2019, 8, e46564. [Google Scholar] [CrossRef]
- Marko, J.F.; De Los Rios, P.; Barducci, A.; Gruber, S. DNA-segment-capture model for loop extrusion by structural maintenance of chromosome (SMC) protein complexes. Nucleic Acids Res. 2019, 47, 6956–6972. [Google Scholar] [CrossRef]
- Bürmann, F.; Funke, L.F.H.; Chin, J.W.; Löwe, J. Cryo-EM structure of MukBEF reveals DNA loop entrapment at chromosomal unloading sites. Mol. Cell 2021, 81, 4891–4906.e8. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Leonard, A.C. Recollections of a Helmstetter Disciple. Life 2023, 13, 1114. https://doi.org/10.3390/life13051114
Leonard AC. Recollections of a Helmstetter Disciple. Life. 2023; 13(5):1114. https://doi.org/10.3390/life13051114
Chicago/Turabian StyleLeonard, Alan C. 2023. "Recollections of a Helmstetter Disciple" Life 13, no. 5: 1114. https://doi.org/10.3390/life13051114