Abstract
All viable bacterial cells, whether they divide symmetrically or asymmetrically, must coordinate their growth, division, cell volume and shape with the inheritance of the genome. These coordinated processes maintain genome integrity over generations as chromosomes are duplicated and segregated during each cell cycle, and include the organization of DNA into nucleoids, controlled and faithful DNA replication, chromosome unlinking and faithful segregation into daughter cells. In this Review, we explore the contributions of chromosome structure and nucleoid organization to cell cycle regulation, detail the cellular processes involved in the initiation of DNA replication and DNA segregation and explore how those processes are linked to cell growth and cell division. Furthermore, we address how the study of a growing number of bacterial species enables the search for common principles that underlie the coordination of chromosome inheritance with the cell cycle.
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References
Willis, L. & Huang, K. C. Sizing up the bacterial cell cycle. Nat. Rev. Microbiol. 15, 606–620 (2017).
Schneiker, S. et al. Complete genome sequence of the myxobacterium Sorangium cellulosum. Nat. Biotechnol. 25, 1281–1289 (2007).
Han, K. et al. Extraordinary expansion of a Sorangium cellulosum genome from an alkaline milieu. Sci. Rep. 3, 2101 (2013).
Bennett, G. M. & Moran, N. A. Small, smaller, smallest: the origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biol. Evol. 5, 1675–1688 (2013).
Jun, S. Chromosome, cell cycle, and entropy. Biophys. J. 108, 785–786 (2015).
Stracy, M. et al. Live-cell superresolution microscopy reveals the organization of RNA polymerase in the bacterial nucleoid. Proc. Natl Acad. Sci. USA 112, E4390–E4399 (2015).
Reyes-Lamothe, R., Nicolas, E. & Sherratt, D. J. Chromosome replication and segregation in bacteria. Annu. Rev. Genet. 46, 121–143 (2012).
Wang, X., Montero Llopis, P. & Rudner, D. Z. Bacillus subtilis chromosome organization oscillates between two distinct patterns. Proc. Natl Acad. Sci. USA 111, 12877–12882 (2014).
Badrinarayanan, A., Le, T. B. & Laub, M. T. Bacterial chromosome organization and segregation. Annu. Rev. Cell Dev. Biol. 31, 171–199 (2015).
den Blaauwen, T. Prokaryotic cell division: flexible and diverse. Curr. Opin. Microbiol. 16, 738–744 (2013).
Sauls, J. T., Li, D. & Jun, S. Adder and a coarse-grained approach to cell size homeostasis in bacteria. Curr. Opin. Cell Biol. 38, 38–44 (2016).
Schaechter, M., Bentzon, M. W. & Maaloe, O. Synthesis of deoxyribonucleic acid during the division cycle of bacteria. Nature 183, 1207–1208 (1959).
Cooper, S. & Helmstetter, C. E. Chromosome replication and the division cycle of Escherichia coli B/r. J. Mol. Biol. 31, 519–540 (1968).
Donachie, W. D. Relationship between cell size and time of initiation of DNA replication. Nature 219, 1077–1079 (1968).
Dubarry, N., Willis, C. R., Ball, G., Lesterlin, C. & Armitage, J. P. In vivo imaging of the segregation of the 2 chromosomes and the cell division proteins of Rhodobacter sphaeroides reveals an unexpected role for MipZ. mBio 10, e02515-18 (2019).
Collier, J. Regulation of chromosomal replication in Caulobacter crescentus. Plasmid 67, 76–87 (2012).
Helmstetter, C., Cooper, S., Pierucci, O. & Revelas, E. On the bacterial life sequence. Cold Spring Harb. Symp. Quant. Biol. 33, 809–822 (1968).
Stokke, C., Waldminghaus, T. & Skarstad, K. Replication patterns and organization of replication forks in Vibrio cholerae. Microbiology 157, 695–708 (2011).
Lindas, A. C. & Bernander, R. The cell cycle of archaea. Nat. Rev. Microbiol. 11, 627–638 (2013).
Si, F. et al. Invariance of initiation mass and predictability of cell size in Escherichia coli. Curr. Biol. 27, 1278–1287 (2017).
Zheng, H. et al. Interrogating the Escherichia coli cell cycle by cell dimension perturbations. Proc. Natl Acad. Sci. USA 113, 15000–15005 (2016).
Wallden, M., Fange, D., Lundius, E. G., Baltekin, O. & Elf, J. The synchronization of replication and division cycles in individual E. coli cells. Cell 166, 729–739 (2016).
Whitman, W. B., Coleman, D. C. & Wiebe, W. J. Prokaryotes: the unseen majority. Proc. Natl Acad. Sci. USA 95, 6578–6583 (1998).
Lomstein, B. A., Langerhuus, A. T., D’Hondt, S., Jorgensen, B. B. & Spivack, A. J. Endospore abundance, microbial growth and necromass turnover in deep sub-seafloor sediment. Nature 484, 101–104 (2012).
Rocha, E. P. & Danchin, A. Essentiality, not expressiveness, drives gene-strand bias in bacteria. Nat. Genet. 34, 377–378 (2003).
Rocha, E. P. & Danchin, A. Gene essentiality determines chromosome organisation in bacteria. Nucleic Acids Res. 31, 6570–6577 (2003).
De Septenville, A. L., Duigou, S., Boubakri, H. & Michel, B. Replication fork reversal after replication-transcription collision. PLOS Genet. 8, e1002622 (2012).
Wang, J. D., Berkmen, M. B. & Grossman, A. D. Genome-wide coorientation of replication and transcription reduces adverse effects on replication in Bacillus subtilis. Proc. Natl Acad. Sci. USA 104, 5608–5613 (2007).
Bremer, H. & Dennis, P. P. Modulation of chemical composition and other parameters of the cell at different exponential growth rates. EcoSal Plus https://doi.org/10.1128/ecosal.5.2.3 (2008).
Couturier, E. & Rocha, E. P. Replication-associated gene dosage effects shape the genomes of fast-growing bacteria but only for transcription and translation genes. Mol. Microbiol. 59, 1506–1518 (2006).
Touzain, F., Petit, M. A., Schbath, S. & El Karoui, M. DNA motifs that sculpt the bacterial chromosome. Nat. Rev. Microbiol. 9, 15–26 (2011).
Woldringh, C. L. & Nanninga, N. Structural and physical aspects of bacterial chromosome segregation. J. Struct. Biol. 156, 273–283 (2006).
Paulson, J. R. & Laemmli, U. K. The structure of histone-depleted metaphase chromosomes. Cell 12, 817–828 (1977).
Kavenoff, R. & Bowen, B. C. Electron microscopy of membrane-free folded chromosomes from Escherichia coli. Chromosoma 59, 89–101 (1976).
Wang, X., Possoz, C. & Sherratt, D. J. Dancing around the divisome: asymmetric chromosme segregation in Escherichia coli. Genes Dev. 19, 2367–2377 (2005).
Nielsen, H. J., Li, Y., Youngren, B., Hansen, F. G. & Austin, S. Progressive segregation of the Escherichia coli chromosome. Mol. Microbiol. 61, 383–393 (2006).
Viollier, P. H. et al. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc. Natl Acad. Sci. USA 101, 9257–9262 (2004).
Vallet-Gely, I. & Boccard, F. Chromosomal organization and segregation in Pseudomonas aeruginosa. PLOS Genet. 9, e1003492 (2013).
David, A. et al. The two cis-acting sites, parS1 and oriC1, contribute to the longitudinal organisation of Vibrio cholerae chromosome I. PLOS Genet. 10, e1004448 (2014).
Nasmyth, K. & Haering, C. H. The structure and function of SMC and kleisin complexes. Annu. Rev. Biochem. 74, 595–648 (2005).
Ganji, M. et al. Real-time imaging of DNA loop extrusion by condensin. Science 360, 102–105 (2018).
Mercier, R. et al. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135, 475–485 (2008).
Lioy, V. S. et al. Multiscale structuring of the E. coli chromosome by nucleoid-associated and condensin proteins. Cell 172, 771–783 (2018).
Nolivos, S. et al. MatP regulates the coordinated action of topoisomerase IV and MukBEF in chromosome segregation. Nat. Commun. 7, 10466 (2016).
Niki, H., Jaffe, A., Imamura, R., Ogura, T. & Hiraga, S. The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J. 10, 183–193 (1991).
Duderstadt, K. E. & Berger, J. M. AAA+ ATPases in the initiation of DNA replication. Crit. Rev. Biochem. Mol. Biol. 43, 163–187 (2008).
Wolanski, M., Donczew, R., Zawilak-Pawlik, A. & Zakrzewska-Czerwinska, J. oriC-encoded instructions for the initiation of bacterial chromosome replication. Front. Microbiol. 5, 735 (2014).
Grimwade, J. E. et al. Origin recognition is the predominant role for DnaA-ATP in initiation of chromosome replication. Nucleic Acids Res. 46, 6140–6151 (2018).
McGarry, K. C., Ryan, V. T., Grimwade, J. E. & Leonard, A. C. Two discriminatory binding sites in the Escherichia coli replication origin are required for DNA strand opening by initiator DnaA-ATP. Proc. Natl Acad. Sci. USA 101, 2811–2816 (2004).
Kawakami, H., Keyamura, K. & Katayama, T. Formation of an ATP-DnaA-specific initiation complex requires DnaA Arginine 285, a conserved motif in the AAA+ protein family. J. Biol. Chem. 280, 27420–27430 (2005).
Rozgaja, T. A. et al. Two oppositely oriented arrays of low-affinity recognition sites in oriC guide progressive binding of DnaA during Escherichia coli pre-RC assembly. Mol. Microbiol. 82, 475–488 (2011).
Stepankiw, N., Kaidow, A., Boye, E. & Bates, D. The right half of the Escherichia coli replication origin is not essential for viability, but facilitates multi-forked replication. Mol. Microbiol. 74, 467–479 (2009).
Sakiyama, Y., Kasho, K., Noguchi, Y., Kawakami, H. & Katayama, T. Regulatory dynamics in the ternary DnaA complex for initiation of chromosomal replication in Escherichia coli. Nucleic Acids Res. 45, 12354–12373 (2017).
Kowalski, D. & Eddy, M. J. The DNA unwinding element: a novel, cis-acting component that facilitates opening of the Escherichia coli replication origin. EMBO J. 8, 4335–4344 (1989).
Kaur, G. et al. Building the bacterial orisome: high-affinity DnaA recognition plays a role in setting the conformation of oriC DNA. Mol. Microbiol. 91, 1148–1163 (2014).
Kurokawa, K., Nishida, S., Emoto, A., Sekimizu, K. & Katayama, T. Replication cycle-coordinated change of the adenine nucleotide-bound forms of DnaA protein in Escherichia coli. EMBO J. 18, 6642–6652 (1999).
Kato, J. & Katayama, T. Hda, a novel DnaA-related protein, regulates the replication cycle in Escherichia coli. EMBO J. 20, 4253–4262 (2001).
Kasho, K., Tanaka, H., Sakai, R. & Katayama, T. Cooperative DnaA binding to the negatively supercoiled datA locus stimulates DnaA-ATP hydrolysis. J. Biol. Chem. 292, 1251–1266 (2017).
Fujimitsu, K., Senriuchi, T. & Katayama, T. Specific genomic sequences of E. coli promote replicational initiation by directly reactivating ADP-DnaA. Genes Dev. 23, 1221–1233 (2009).
Sekimizu, K. & Kornberg, A. Cardiolipin activation of dnaA protein, the initiation protein of replication in Escherichia coli. J. Biol. Chem. 263, 7131–7135 (1988).
Flatten, I., Fossum-Raunehaug, S., Taipale, R., Martinsen, S. & Skarstad, K. The DnaA protein is not the limiting factor for initiation of replication in Escherichia coli. PLOS Genet. 11, e1005276 (2015).
Campbell, J. L. & Kleckner, N. E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62, 967–979 (1990).
Nievera, C., Torgue, J. J., Grimwade, J. E. & Leonard, A. C. SeqA blocking of DnaA-oriC interactions ensures staged assembly of the E. coli pre-RC. Mol. Cell 24, 581–592 (2006).
Leonard, A. C. & Grimwade, J. E. The orisome: structure and function. Front. Microbiol. 6, 545 (2015).
Hansen, F. G. & Atlung, T. The DnaA tale. Front. Microbiol. 9, 319 (2018).
Katayama, T., Kasho, K. & Kawakami, H. The DnaA cycle in Escherichia coli: activation, function and inactivation of the initiator protein. Front. Microbiol. 8, 2496 (2017).
Skarstad, K. & Katayama, T. Regulating DNA replication in bacteria. Cold Spring Harb. Perspect. Biol. 5, a012922 (2013).
Kurokawa, K. et al. Rapid exchange of bound ADP on the Staphylococcus aureus replication initiation protein DnaA. J. Biol. Chem. 284, 34201–34210 (2009).
Scholefield, G. & Murray, H. YabA and DnaD inhibit helix assembly of the DNA replication initiation protein DnaA. Mol. Microbiol. 90, 147–159 (2013).
Scholefield, G., Errington, J. & Murray, H. Soj/ParA stalls DNA replication by inhibiting helix formation of the initiator protein DnaA. EMBO J. 31, 1542–1555 (2012).
Collier, J. & Shapiro, L. Feedback control of DnaA-mediated replication initiation by replisome-associated HdaA protein in Caulobacter. J. Bacteriol. 191, 5706–5716 (2009).
Wargachuk, R. & Marczynski, G. T. The Caulobacter crescentus homolog of DnaA (HdaA) also regulates the proteolysis of the replication initiator protein DnaA. J. Bacteriol. 197, 3521–3532 (2015).
Jonas, K., Chen, Y. E. & Laub, M. T. Modularity of the bacterial cell cycle enables independent spatial and temporal control of DNA replication. Curr. Biol. 21, 1092–1101 (2011).
Bastedo, D. P. & Marczynski, G. T. CtrA response regulator binding to the Caulobacter chromosome replication origin is required during nutrient and antibiotic stress as well as during cell cycle progression. Mol. Microbiol. 72, 139–154 (2009).
Val, M. E., Soler-Bistue, A., Bland, M. J. & Mazel, D. Management of multipartite genomes: the Vibrio cholerae model. Curr. Opin. Microbiol. 22, 120–126 (2014).
Nordstrom, K. & Dasgupta, S. Copy-number control of the Escherichia coli chromosome: a plasmidologist’s view. EMBO Rep. 7, 484–489 (2006).
Tolmasky, M. & Alonso, J. C. Plasmids: Biology and Impact in Biotechnology and Discovery (ASM Press, 2015).
Rasmussen, T., Jensen, R. B. & Skovgaard, O. The two chromosomes of Vibrio cholerae are initiated at different time points in the cell cycle. EMBO J. 26, 3124–3131 (2007).
Frage, B. et al. Spatiotemporal choreography of chromosome and megaplasmids in the Sinorhizobium meliloti cell cycle. Mol. Microbiol. 100, 808–823 (2016).
Deghelt, M. et al. G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus. Nat. Commun. 5, 4366 (2014).
Du, W. L. et al. Orderly replication and segregation of the four replicons of Burkholderia cenocepacia J2315. PLOS Genet. 12, e1006172 (2016).
Baek, J. H. & Chattoraj, D. K. Chromosome I controls chromosome II replication in Vibrio cholerae. PLOS Genet. 10, e1004184 (2014).
Pal, D., Venkova-Canova, T., Srivastava, P. & Chattoraj, D. K. Multipartite regulation of rctB, the replication initiator gene of Vibrio cholerae chromosome II. J. Bacteriol. 187, 7167–7175 (2005).
Duigou, S. et al. Independent control of replication initiation of the two Vibrio cholerae chromosomes by DnaA and RctB. J. Bacteriol. 188, 6419–6424 (2006).
Val, M. E. et al. A checkpoint control orchestrates the replication of the two chromosomes of Vibrio cholerae. Sci. Adv. 2, e1501914 (2016).
Griese, M., Lange, C. & Soppa, J. Ploidy in cyanobacteria. FEMS Microbiol. Lett. 323, 124–131 (2011).
Ohbayashi, R. et al. DNA replication depends on photosynthetic electron transport in cyanobacteria. FEMS Microbiol. Lett. 344, 138–144 (2013).
Watanabe, S. et al. Light-dependent and asynchronous replication of cyanobacterial multi-copy chromosomes. Mol. Microbiol. 83, 856–865 (2012).
Chen, A. H., Afonso, B., Silver, P. A. & Savage, D. F. Spatial and temporal organization of chromosome duplication and segregation in the cyanobacterium Synechococcus elongatus PCC 7942. PLOS ONE 7, e47837 (2012).
Jain, I. H., Vijayan, V. & O’Shea, E. K. Spatial ordering of chromosomes enhances the fidelity of chromosome partitioning in cyanobacteria. Proc. Natl Acad. Sci. USA 109, 13638–13643 (2012).
Paijmans, J., Bosman, M., Ten Wolde, P. R. & Lubensky, D. K. Discrete gene replication events drive coupling between the cell cycle and circadian clocks. Proc. Natl Acad. Sci. USA 113, 4063–4068 (2016).
Mendell, J. E., Clements, K. D., Choat, J. H. & Angert, E. R. Extreme polyploidy in a large bacterium. Proc. Natl Acad. Sci. USA 105, 6730–6734 (2008).
Kornberg, A. & Baker, T. DNA Replication 2nd edn (Freeman, 1992).
Trojanowski, D. et al. Choreography of the Mycobacterium replication machinery during the cell cycle. mBio 6, e02125-14 (2015).
Churchward, G. & Bremer, H. Determination of deoxyribonucleic acid replication time in exponentially growing Escherichia coli B/r. J. Bacteriol. 130, 1206–1213 (1977).
Allman, R., Schjerven, T. & Boye, E. Cell cycle parameters of Escherichia coli K-12. J. Bacteriol. 173, 7970–7974 (1991).
Lewis, J. S., Jergic, S. & Dixon, N. E. The E. coli DNA replication fork. Enzymes 39, 31–88 (2016).
Beattie, T. R. & Reyes-Lamothe, R. A replisome’s journey through the bacterial chromosome. Front. Microbiol. 6, 562 (2015).
Beattie, T. R. et al. Frequent exchange of the DNA polymerase during bacterial chromosome replication. eLife 6, e21763 (2017).
Lewis, J. S. et al. Single-molecule visualization of fast polymerase turnover in the bacterial replisome. Elife 6, e23932 (2017).
Liao, Y., Li, Y., Schroeder, J. W., Simmons, L. A. & Biteen, J. S. Single-molecule DNA polymerase dynamics at a bacterial replisome in live cells. Biophys. J. 111, 2562–2569 (2016).
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).
Zaritsky, A. & Pritchard, R. H. Changes in cell size and shape associated with changes in the replication time of the chromosome of Escherichia coli. J. Bacteriol. 114, 824–837 (1973).
Morigen, Odsbu,I. & Skarstad, K. A reduction in ribonucleotide reductase activity slows down the chromosome replication fork but does not change its localization. PLOS ONE 4, e7617 (2009).
Zhu, M. et al. Manipulating the bacterial cell cycle and cell size by titrating the expression of ribonucleotide reductase. mBio 8, e01741-17 (2017).
Olliver, A., Saggioro, C., Herrick, J. & Sclavi, B. DnaA-ATP acts as a molecular switch to control levels of ribonucleotide reductase expression in Escherichia coli. Mol. Microbiol. 76, 1555–1571 (2010).
Hanke, P. D. & Fuchs, J. A. Regulation of ribonucleoside diphosphate reductase mRNA synthesis in. Escherichia coli. J. Bacteriol. 154, 1040–1045 (1983).
Torrents, E. et al. NrdR controls differential expression of the Escherichia coli ribonucleotide reductase genes. J. Bacteriol. 189, 5012–5021 (2007).
Gon, S. et al. A novel regulatory mechanism couples deoxyribonucleotide synthesis and DNA replication in Escherichia coli. EMBO J. 25, 1137–1147 (2006).
Babu, V. M. P., Itsko, M., Baxter, J. C., Schaaper, R. M. & Sutton, M. D. Insufficient levels of the nrdAB-encoded ribonucleotide reductase underlie the severe growth defect of the Deltahda E. coli strain. Mol. Microbiol. 104, 377–399 (2017).
McKethan, B. L. & Spiro, S. Cooperative and allosterically controlled nucleotide binding regulates the DNA binding activity of NrdR. Mol. Microbiol. 90, 278–289 (2013).
Denapoli, J., Tehranchi, A. K. & Wang, J. D. Dose-dependent reduction of replication elongation rate by (p)ppGpp in Escherichia coli and Bacillus subtilis. Mol. Microbiol. 88, 93–104 (2013).
Wang, J. D., Sanders, G. M. & Grossman, A. D. Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128, 865–875 (2007).
Christensen, R. B., Christensen, J. R., Koenig, I. & Lawrence, C. W. Untargeted mutagenesis induced by UV in the lacI gene of Escherichia coli. Mol. Gen. Genet. 201, 30–34 (1985).
Wendel, B. M., Cole, J. M., Courcelle, C. T. & Courcelle, J. SbcC-SbcD and ExoI process convergent forks to complete chromosome replication. Proc. Natl Acad. Sci. USA 115, 349–354 (2018).
Midgley-Smith, S. L. et al. Chromosomal over-replication in Escherichia coli recG cells is triggered by replication fork fusion and amplified if replichore symmetry is disturbed. Nucleic Acids Res. 46, 7701–7715 (2018).
Sinha, A. K. et al. Division-induced DNA double strand breaks in the chromosome terminus region of Escherichia coli lacking RecBCD DNA repair enzyme. PLOS Genet. 13, e1006895 (2017).
Wang, X., Montero Llopis, P. & Rudner, D. Z. Organization and segregation of bacterial chromosomes. Nat. Rev. Genet. 14, 191–203 (2013).
Adams, D. W., Wu, L. J. & Errington, J. Cell cycle regulation by the bacterial nucleoid. Curr. Opin. Microbiol. 22, 94–101 (2014).
Postow, L., Crisona, N. J., Peter, B. J., Hardy, C. D. & Cozzarelli, N. R. Topological challenges to DNA replication: conformations at the fork. Proc. Natl Acad. Sci. USA 98, 8219–8226 (2001).
Wang, X., Reyes-Lamothe, R. & Sherratt, D. J. Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev. 22, 2426–2433 (2008).
Joshi, M. C. et al. Regulation of sister chromosome cohesion by the replication fork tracking protein SeqA. PLOS Genet. 9, e1003673 (2013).
Barre, F. X. & Sherratt, D. in The Bacterial Chromosome Ch. 28 (ed. Higgins, N. P.) 513–524 (ASM Press, 2005).
Ip, S. C., Bregu, M., Barre, F. X. & Sherratt, D. J. Decatenation of DNA circles by FtsK-dependent Xer site-specific recombination. EMBO J. 22, 6399–6407 (2003).
Grainge, I. et al. Unlinking chromosome catenanes in vivo by site-specific recombination. EMBO J. 26, 4228–4238 (2007).
Jun, S. & Wright, A. Entropy as the driver of chromosome segregation. Nat. Rev. Microbiol. 8, 600–607 (2010).
Kennedy, S. P., Chevalier, F. & Barre, F. X. Delayed activation of Xer recombination at dif by FtsK during septum assembly in Escherichia coli. Mol. Microbiol. 68, 1018–1028 (2008).
Hobbie, J. E. & Hobbie, E. A. Microbes in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimating microbial rates. Front. Microbiol. 4, 324 (2013).
Slager, J., Kjos, M., Attaiech, L. & Veening, J. W. Antibiotic-induced replication stress triggers bacterial competence by increasing gene dosage near the origin. Cell 157, 395–406 (2014).
Ohbayashi, R. et al. Diversification of DnaA dependency for DNA replication in cyanobacterial evolution. ISME J. 10, 1113–1121 (2016).
Errington, J. L-Form bacteria, cell walls and the origins of life. Open Biol. 3, 120143 (2013).
Potvin-Trottier, L., Luro, S. & Paulsson, J. Microfluidics and single-cell microscopy to study stochastic processes in bacteria. Curr. Opin. Microbiol. 43, 186–192 (2018).
Ullman, G. et al. High-throughput gene expression analysis at the level of single proteins using a microfluidic turbidostat and automated cell tracking. Phil. Trans. R. Soc. B 368, 20120025 (2013).
Uphoff, S. et al. Stochastic activation of a DNA damage response causes cell-to-cell mutation rate variation. Science 351, 1094–1097 (2016).
Liu, J. et al. Coupling between distant biofilms and emergence of nutrient time-sharing. Science 356, 638–642 (2017).
Din, M. O. et al. Synchronized cycles of bacterial lysis for in vivo delivery. Nature 536, 81–85 (2016).
Massalha, H., Korenblum, E., Malitsky, S., Shapiro, O. H. & Aharoni, A. Live imaging of root-bacteria interactions in a microfluidics setup. Proc. Natl Acad. Sci. USA 114, 4549–4554 (2017).
Walsh, E. J. et al. Microfluidics with fluid walls. Nat. Commun. 8, 816 (2017).
Lawson, M. J. et al. In situ genotyping of a pooled strain library after characterizing complex phenotypes. Mol. Syst. Biol. 13, 947 (2017).
Campos, M. et al. Genomewide phenotypic analysis of growth, cell morphogenesis, and cell cycle events in Escherichia coli. Mol. Syst. Biol. 14, e7573 (2018).
Helmstetter, C. E. DNA synthesis during the division cycle of rapidly growing Escherichia coli B/r. J. Mol. Biol. 31, 507–518 (1968).
Skarstad, K., Boye, E. & Steen, H. B. Timing of initiation of chromosome replication in individual Escherichia coli cells. EMBO J. 5, 1711–1717 (1986).
Michelsen, O., Teixeira de Mattos, M. J., Jensen, P. R. & Hansen, F. G. Precise determinations of C and D periods by flow cytometry in Escherichia coli K-12 and B/r. Microbiology 149, 1001–1010 (2003).
Reyes-Lamothe, R., Possoz, C., Danilova, O. & Sherratt, D. J. Independent positioning and action of Escherichia coli replisomes in live cells. Cell 133, 90–102 (2008).
Jensen, R. B., Wang, S. C. & Shapiro, L. A moving DNA replication factory in Caulobacter crescentus. EMBO J. 20, 4952–4963 (2001).
Cook, P. R. The organization of replication and transcription. Science 284, 1790–1795 (1999).
Lemon, K. P. & Grossman, A. D. Localization of bacterial DNA polymerase: evidence for a factory model of replication. Science 282, 1516–1519 (1998).
Mangiameli, S. M., Veit, B. T., Merrikh, H. & Wiggins, P. A. The replisomes remain spatially proximal throughout the cell cycle in bacteria. PLOS Genet. 13, e1006582 (2017).
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).
Arias-Cartin, R. et al. Replication fork passage drives asymmetric dynamics of a critical nucleoid-associated protein in Caulobacter. EMBO J. 36, 301–318 (2017).
Breier, A. M., Weier, H.-U. G. & Cozzarelli, N. R. Independence of replisomes in Escherichia coli chromosomal replication. Proc. Natl Acad. Sci. USA 102, 3942–3947 (2005).
Bates, D. & Kleckner, N. Chromosome and replisome dynamics in E. coli: loss of sister cohesion triggers global chromosome movement and mediates chromosome segregation. Cell 121, 899–911 (2005).
Skarstad, K., Steen, H. B. & Boye, E. Cell cycle parameters of slowly growing Escherichia coli B/r studied by flow cytometry. J. Bacteriol. 154, 656–662 (1983).
Skarstad, K., Steen, H. B. & Boye, E. Escherichia coli DNA distributions measured by flow cytometry and compared with theoretical computer simulations. J. Bacteriol. 163, 661–668 (1985).
Marczynski, G. T., Dingwall, A. & Shapiro, L. Plasmid and chromosomal DNA replication and partitioning during the Caulobacter crescentus cell cycle. J. Mol. Biol. 212, 709–722 (1990).
Le, T. B., Imakaev, M. V., Mirny, L. A. & Laub, M. T. High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342, 731–734 (2013).
Acknowledgements
Research in the Reyes-Lamothe laboratory is funded by the Natural Sciences and Engineering Research Council of Canada (NSERC# 435521–2013), the Canadian Institutes for Health Research (CIHR MOP# 142473) and the Canada Research Chairs programme. The Sherratt laboratory is funded by a Wellcome Investigator Award (200782/Z/16/Z). The authors thank many colleagues for stimulating discussions, in particular S. Uphoff and B. Novak (University of Oxford) and members of the Reyes-Lamothe laboratory.
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Nature Reviews Microbiology thanks T. Katayama and the other anonymous reviewer(s) for their contribution to the peer review of this work.
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R.R.-L. and D.J.S. researched data for the article, substantially contributed to the discussion of content, wrote the article and reviewed and edited the article before submission.
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Glossary
- Replichores
-
Two chromosomal halves starting at the replication origin, each replicated by a different replication fork.
- Generation time
-
Average time from birth to division.
- Replication forks
-
Y-shaped DNA structures formed at the point where DNA is unwound during DNA replication.
- Nucleoid occlusion
-
The process by which the presence of nucleoid DNA prevents the formation of an FtsZ ring and divisome over that DNA.
- Stalked cells
-
Sessile, proliferative Caulobacter crescentus cells.
- Swarmer cells
-
Motile Caulobacter crescentus cells that do not replicate.
- Iteron plasmids
-
Characterized by a replication origin composed of repeated sequences that bind to a cognate initiator protein.
- Primase
-
Replisome subunit that synthesizes short RNA primers which are then elongated by the DNA polymerase.
- SOS response
-
Cellular response to DNA damage leading to inhibition of cell division and induction of DNA repair systems.
- Divisome
-
Structure that forms around the middle of the cell, composed of multiple proteins required for cell division.
- Cohesion time
-
Time from the replication of a locus to the separation of the newly replicated sister loci.
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Reyes-Lamothe, R., Sherratt, D.J. The bacterial cell cycle, chromosome inheritance and cell growth. Nat Rev Microbiol 17, 467–478 (2019). https://doi.org/10.1038/s41579-019-0212-7
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DOI: https://doi.org/10.1038/s41579-019-0212-7
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