Cell cycle‐dependent regulation of FtsZ in Escherichia coli in slow growth conditions

Männik, Jaana; Walker, Bryant E.; Männik, Jaan

doi:10.1111/mmi.14135

Title: Cell cycle‐dependent regulation of FtsZ in Escherichia coli in slow growth conditions

Journal Article · 28 October 2018 · Molecular Microbiology

DOI: https://doi.org/10.1111/mmi.14135 · OSTI ID:1479823

^[1]; Walker, Bryant E. ^[2];

^[2]

Department of Biochemistry &, Cellular and Molecular Biology University of Tennessee Knoxville TN 37996 USA
Department of Physics and Astronomy University of Tennessee Knoxville TN 37996 USA

Summary FtsZ is the key regulator of bacterial cell division. It initiates division by forming a dynamic ring‐like structure, the Z‐ring, at the mid‐cell. What triggers the formation of the Z‐ring during the cell cycle is poorly understood. In Escherichia coli , the common view is that FtsZ concentration is constant throughout its doubling time and therefore regulation of assembly is controlled by some yet‐to‐be‐identified protein‐protein interactions. Using a newly developed functional, fluorescent FtsZ reporter, we performed a quantitative analysis of the FtsZ concentration throughout the cell cycle under slow growth conditions. In contrast to the common expectation, we show that FtsZ concentrations vary in a cell cycle‐dependent manner, and that upregulation of FtsZ synthesis correlates with the formation of the Z‐ring. The first half of the cell cycle shows an approximately fourfold upregulation of FtsZ synthesis, followed by its rapid degradation by ClpXP protease in the last 10% of the cell cycle. The initiation of rapid degradation coincides with the dissociation of FtsZ from the septum. Altogether, our data suggest that the Z‐ring formation in slow growth conditions in E. coli is partially controlled by a regulatory sequence wherein upregulation of an essential cell cycle factor is followed by its degradation.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1479823

Journal Information:: Molecular Microbiology, Journal Name: Molecular Microbiology Journal Issue: 6 Vol. 110; ISSN 0950-382X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: FAO

Language:: English

References (63)

FtsZ condensates: An in vitro electron microscopy study Popp, David; Iwasa, Mitsusada; Narita, Akihiro Biopolymers, Vol. 91, Issue 5 https://doi.org/10.1002/bip.21136	journal	May 2009
Transcription of ftsZ oscillates during the cell cycle of Escherichia coli. Garrido, T.; Sánchez, M.; Palacios, P. The EMBO Journal, Vol. 12, Issue 10 https://doi.org/10.1002/j.1460-2075.1993.tb06073.x	journal	October 1993
Molecular Evolution of FtsZ Protein Sequences Encoded Within the Genomes of Archaea, Bacteria, and Eukaryota Vaughan, Sue; Wickstead, Bill; Gull, Keith Journal of Molecular Evolution, Vol. 58, Issue 1 https://doi.org/10.1007/s00239-003-2523-5	journal	January 2004
Direct Binding of FtsZ to ZipA, an Essential Component of the Septal Ring Structure That Mediates Cell Division in E. coli Hale, Cynthia A.; de Boer, Piet A. J. Cell, Vol. 88, Issue 2 https://doi.org/10.1016/S0092-8674(00)81838-3	journal	January 1997
Proteomic Discovery of Cellular Substrates of the ClpXP Protease Reveals Five Classes of ClpX-Recognition Signals Flynn, Julia M.; Neher, Saskia B.; Kim, Yong-In Molecular Cell, Vol. 11, Issue 3 https://doi.org/10.1016/S1097-2765(03)00060-1	journal	March 2003
Coordination of Cell Division and Chromosome Segregation by a Nucleoid Occlusion Protein in Bacillus subtilis Wu, Ling Juan; Errington, Jeff Cell, Vol. 117, Issue 7 https://doi.org/10.1016/j.cell.2004.06.002	journal	June 2004
Chromosome and Replisome Dynamics in E. coli: Loss of Sister Cohesion Triggers Global Chromosome Movement and Mediates Chromosome Segregation Bates, David; Kleckner, Nancy Cell, Vol. 121, Issue 6 https://doi.org/10.1016/j.cell.2005.04.013	journal	June 2005
Real-Time Kinetics of Gene Activity in Individual Bacteria Golding, Ido; Paulsson, Johan; Zawilski, Scott M. Cell, Vol. 123, Issue 6 https://doi.org/10.1016/j.cell.2005.09.031	journal	December 2005
ClpX(P) Generates Mechanical Force to Unfold and Translocate Its Protein Substrates Maillard, Rodrigo A.; Chistol, Gheorghe; Sen, Maya Cell, Vol. 145, Issue 3 https://doi.org/10.1016/j.cell.2011.04.010	journal	April 2011
Robust Growth of Escherichia coli Wang, Ping; Robert, Lydia; Pelletier, James Current Biology, Vol. 20, Issue 12 https://doi.org/10.1016/j.cub.2010.04.045	journal	June 2010
Advances in understanding E. coli cell fission de Boer, Piet AJ Current Opinion in Microbiology, Vol. 13, Issue 6 https://doi.org/10.1016/j.mib.2010.09.015	journal	December 2010
Cell cycle regulation by the bacterial nucleoid Adams, David William; Wu, Ling Juan; Errington, Jeff Current Opinion in Microbiology, Vol. 22 https://doi.org/10.1016/j.mib.2014.09.020	journal	December 2014
Cell cycle control in Alphaproteobacteria Collier, Justine Current Opinion in Microbiology, Vol. 30 https://doi.org/10.1016/j.mib.2016.01.010	journal	April 2016
SlmA, a Nucleoid-Associated, FtsZ Binding Protein Required for Blocking Septal Ring Assembly over Chromosomes in E. coli Bernhardt, Thomas G.; de Boer, Piet A. J. Molecular Cell, Vol. 18, Issue 5 https://doi.org/10.1016/j.molcel.2005.04.012	journal	May 2005
Strong FtsZ is with the force: mechanisms to constrict bacteria Mingorance, Jesús; Rivas, Germán; Vélez, Marisela Trends in Microbiology, Vol. 18, Issue 8 https://doi.org/10.1016/j.tim.2010.06.001	journal	August 2010
FtsZ ring structure associated with division in Escherichia coli Bi, Erfei; Lutkenhaus, Joe Nature, Vol. 354, Issue 6349 https://doi.org/10.1038/354161a0	journal	November 1991
Ribosome degradation in growing bacteria Piir, Kerli; Paier, Anton; Liiv, Aivar EMBO reports, Vol. 12, Issue 5 https://doi.org/10.1038/embor.2011.47	journal	April 2011
The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns Loose, Martin; Mitchison, Timothy J. Nature Cell Biology, Vol. 16, Issue 1 https://doi.org/10.1038/ncb2885	journal	December 2013
Systematic characterization of maturation time of fluorescent proteins in living cells Balleza, Enrique; Kim, J. Mark; Cluzel, Philippe Nature Methods, Vol. 15, Issue 1 https://doi.org/10.1038/nmeth.4509	journal	November 2017
Splitsville: structural and functional insights into the dynamic bacterial Z ring Haeusser, Daniel P.; Margolin, William Nature Reviews Microbiology, Vol. 14, Issue 5 https://doi.org/10.1038/nrmicro.2016.26	journal	April 2016
Sizing up the bacterial cell cycle Willis, Lisa; Huang, Kerwyn Casey Nature Reviews Microbiology, Vol. 15, Issue 10 https://doi.org/10.1038/nrmicro.2017.79	journal	August 2017
Bacterial cell division: assembly, maintenance and disassembly of the Z ring Adams, David W.; Errington, Jeff Nature Reviews Microbiology, Vol. 7, Issue 9 https://doi.org/10.1038/nrmicro2198	journal	September 2009
From the regulation of peptidoglycan synthesis to bacterial growth and morphology Typas, Athanasios; Banzhaf, Manuel; Gross, Carol A. Nature Reviews Microbiology, Vol. 10, Issue 2 https://doi.org/10.1038/nrmicro2677	journal	December 2011
ClpXP protease degrades the cytoskeletal protein, FtsZ, and modulates FtsZ polymer dynamics Camberg, J. L.; Hoskins, J. R.; Wickner, S. Proceedings of the National Academy of Sciences, Vol. 106, Issue 26 https://doi.org/10.1073/pnas.0904886106	journal	June 2009
FtsK actively segregates sister chromosomes in Escherichia coli Stouf, M.; Meile, J. -C.; Cornet, F. Proceedings of the National Academy of Sciences, Vol. 110, Issue 27 https://doi.org/10.1073/pnas.1304080110	journal	June 2013
Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ Cordell, S. C.; Robinson, E. J. H.; Lowe, J. Proceedings of the National Academy of Sciences, Vol. 100, Issue 13 https://doi.org/10.1073/pnas.1330742100	journal	June 2003
Cell cycle regulation and cell type-specific localization of the FtsZ division initiation protein in Caulobacter. Quardokus, E.; Din, N.; Brun, Y. V. Proceedings of the National Academy of Sciences, Vol. 93, Issue 13 https://doi.org/10.1073/pnas.93.13.6314	journal	June 1996
A Specific Role for the ZipA Protein in Cell Division: STABILIZATION OF THE FtsZ PROTEIN Pazos, Manuel; Natale, Paolo; Vicente, Miguel Journal of Biological Chemistry, Vol. 288, Issue 5 https://doi.org/10.1074/jbc.M112.434944	journal	December 2012
Complete set of ORF clones of Escherichia coli ASKA library (A Complete Set of E. coli K-12 ORF Archive): Unique Resources for Biological Research Kitagawa, M.; Ara, T.; Arifuzzaman, M. DNA Research, Vol. 12, Issue 5 https://doi.org/10.1093/dnares/dsi012	journal	January 2006
An integrative view of cell cycle control in Escherichia coli Dewachter, Liselot; Verstraeten, Natalie; Fauvart, Maarten FEMS Microbiology Reviews, Vol. 42, Issue 2 https://doi.org/10.1093/femsre/fuy005	journal	January 2018
Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter Kelly, A. J.; Sackett, M. J.; Din, N. Genes & Development, Vol. 12, Issue 6 https://doi.org/10.1101/gad.12.6.880	journal	March 1998
The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system Gottesman, S.; Roche, E.; Zhou, Y. Genes & Development, Vol. 12, Issue 9 https://doi.org/10.1101/gad.12.9.1338	journal	May 1998
Transcriptional regulation of ceil division genes in Escherichia coli Dewar, S. J.; Kagan-Zur, V.; Begg, K. J. Molecular Microbiology, Vol. 3, Issue 10 https://doi.org/10.1111/j.1365-2958.1989.tb00118.x	journal	October 1989
Maturation of the Escherichia coli divisome occurs in two steps : Maturation of the divisome Aarsman, Mirjam E. G.; Piette, André; Fraipont, Claudine Molecular Microbiology, Vol. 55, Issue 6 https://doi.org/10.1111/j.1365-2958.2005.04502.x	journal	January 2005
Influence of the nucleoid and the early stages of DNA replication on positioning the division site in Bacillus subtilis: DNA replication and division site positioning Moriya, S.; Rashid, R. A.; Rodrigues, C. D. Andrade Molecular Microbiology, Vol. 76, Issue 3 https://doi.org/10.1111/j.1365-2958.2010.07102.x	journal	February 2010
Control of division gene expression in Escherichia coli Dewar, Susan J.; Dorazi, Robert FEMS Microbiology Letters, Vol. 187, Issue 1 https://doi.org/10.1111/j.1574-6968.2000.tb09127.x	journal	June 2000
ClpXP and ClpAP proteolytic activity on divisome substrates is differentially regulated following the C aulobacter asymmetric cell division : ClpXP and ClpAP proteolytic activity on divisome substrates Williams, Brandon; Bhat, Nowsheen; Chien, Peter Molecular Microbiology, Vol. 93, Issue 5 https://doi.org/10.1111/mmi.12698	journal	August 2014
Roles for both FtsA and the FtsBLQ subcomplex in FtsN-stimulated cell constriction in E scherichia coli : Cell fission regulation by FtsN, FtsA and FtsBLQ Liu, Bing; Persons, Logan; Lee, Lynda Molecular Microbiology, Vol. 95, Issue 6 https://doi.org/10.1111/mmi.12906	journal	January 2015
Stochastic Gene Expression in a Single Cell Elowitz, M. B. Science, Vol. 297, Issue 5584 https://doi.org/10.1126/science.1070919	journal	August 2002
Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division Bisson-Filho, Alexandre W.; Hsu, Yen-Pang; Squyres, Georgia R. Science, Vol. 355, Issue 6326 https://doi.org/10.1126/science.aak9973	journal	February 2017
GTPase activity–coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis Yang, Xinxing; Lyu, Zhixin; Miguel, Amanda Science, Vol. 355, Issue 6326 https://doi.org/10.1126/science.aak9995	journal	February 2017
Probing for Binding Regions of the FtsZ Protein Surface through Site-Directed Insertions: Discovery of Fully Functional FtsZ-Fluorescent Proteins Moore, Desmond A.; Whatley, Zakiya N.; Joshi, Chandra P. Journal of Bacteriology, Vol. 199, Issue 1 https://doi.org/10.1128/JB.00553-16	journal	October 2016
Investigation of Regulation of FtsZ Assembly by SulA and Development of a Model for FtsZ Polymerization Dajkovic, A.; Mukherjee, A.; Lutkenhaus, J. Journal of Bacteriology, Vol. 190, Issue 7 https://doi.org/10.1128/JB.01612-07	journal	February 2008
Diel Expression of Cell Cycle-Related Genes in Synchronized Cultures of Prochlorococcus sp. Strain PCC 9511 Holtzendorff, J.; Partensky, F.; Jacquet, S. Journal of Bacteriology, Vol. 183, Issue 3 https://doi.org/10.1128/JB.183.3.915-920.2001	journal	February 2001
Independence of Circadian Timing from Cell Division in Cyanobacteria Mori, T.; Johnson, C. H. Journal of Bacteriology, Vol. 183, Issue 8 https://doi.org/10.1128/JB.183.8.2439-2444.2001	journal	April 2001
Concentration and Assembly of the Division Ring Proteins FtsZ, FtsA, and ZipA during the Escherichia coli Cell Cycle Rueda, S.; Vicente, M.; Mingorance, J. Journal of Bacteriology, Vol. 185, Issue 11 https://doi.org/10.1128/JB.185.11.3344-3351.2003	journal	June 2003
Growth Rate-Dependent Regulation of Medial FtsZ Ring Formation Weart, R. B.; Levin, P. A. Journal of Bacteriology, Vol. 185, Issue 9 https://doi.org/10.1128/JB.185.9.2826-2834.2003	journal	May 2003
FtsZ in Bacterial Cytokinesis: Cytoskeleton and Force Generator All in One Erickson, H. P.; Anderson, D. E.; Osawa, M. Microbiology and Molecular Biology Reviews, Vol. 74, Issue 4 https://doi.org/10.1128/MMBR.00021-10	journal	November 2010
Transcription of the ftsZ gene and cell division in Escherichia coli. Robin, A.; Joseleau-Petit, D.; D'Ari, R. Journal of Bacteriology, Vol. 172, Issue 3 https://doi.org/10.1128/jb.172.3.1392-1399.1990	journal	March 1990
Relationship between ftsZ gene expression and chromosome replication in Escherichia coli. Zhou, P.; Helmstetter, C. E. Journal of Bacteriology, Vol. 176, Issue 19 https://doi.org/10.1128/jb.176.19.6100-6106.1994	journal	October 1994
Guanine nucleotide-dependent assembly of FtsZ into filaments. Mukherjee, A.; Lutkenhaus, J. Journal of Bacteriology, Vol. 176, Issue 9 https://doi.org/10.1128/jb.176.9.2754-2758.1994	journal	May 1994
FtsA is localized to the septum in an FtsZ-dependent manner. Addinall, S. G.; Lutkenhaus, J. Journal of Bacteriology, Vol. 178, Issue 24 https://doi.org/10.1128/jb.178.24.7167-7172.1996	journal	December 1996
Mechanical Protein Unfolding and Degradation Olivares, Adrian O.; Baker, Tania A.; Sauer, Robert T. Annual Review of Physiology, Vol. 80, Issue 1 https://doi.org/10.1146/annurev-physiol-021317-121303	journal	February 2018
Assembly Dynamics of the Bacterial Cell Division Protein FtsZ: Poised at the Edge of Stability Romberg, Laura; Levin, Petra Anne Annual Review of Microbiology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.micro.57.012903.074300	journal	October 2003
A Moonlighting Enzyme Links Escherichia coli Cell Size with Central Metabolism Hill, Norbert S.; Buske, Paul J.; Shi, Yue PLoS Genetics, Vol. 9, Issue 7 https://doi.org/10.1371/journal.pgen.1003663	journal	July 2013
Evidence for Divisome Localization Mechanisms Independent of the Min System and SlmA in Escherichia coli Bailey, Matthew W.; Bisicchia, Paola; Warren, Boyd T. PLoS Genetics, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pgen.1004504	journal	August 2014
Kinetics of large-scale chromosomal movement during asymmetric cell division in Escherichia coli Männik, Jaana; Bailey, Matthew W.; O’Neill, Jordan C. PLOS Genetics, Vol. 13, Issue 2 https://doi.org/10.1371/journal.pgen.1006638	journal	February 2017
Location of Dual Sites in E. coli FtsZ Important for Degradation by ClpXP; One at the C-Terminus and One in the Disordered Linker Camberg, Jodi L.; Viola, Marissa G.; Rea, Leslie PLoS ONE, Vol. 9, Issue 4 https://doi.org/10.1371/journal.pone.0094964	journal	April 2014
Spatial coordination between chromosomes and cell division proteins in Escherichia coli Männik, Jaan; Bailey, Matthew W. Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00306	journal	April 2015
Cell age dependent concentration of Escherichia coli divisome proteins analyzed with ImageJ and ObjectJ Vischer, Norbert O. E.; Verheul, Jolanda; Postma, Marten Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00586	journal	June 2015
Analysis of Factors Limiting Bacterial Growth in PDMS Mother Machine Devices Yang, Da; Jennings, Anna D.; Borrego, Evalynn Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00871	journal	May 2018
The Protein Chaperone ClpX Targets Native and Non-native Aggregated Substrates for Remodeling, Disassembly, and Degradation with ClpP LaBreck, Christopher J.; May, Shannon; Viola, Marissa G. Frontiers in Molecular Biosciences, Vol. 4 https://doi.org/10.3389/fmolb.2017.00026	journal	May 2017
Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division Szwedziak, Piotr; Wang, Qing; Bharat, Tanmay A. M. eLife, Vol. 3 https://doi.org/10.7554/eLife.04601	journal	December 2014

Similar Records

High-resolution crystal structures of Escherichia coli FtsZ bound to GDP and GTP

Journal Article · 2020 · Acta Crystallographica. Section F, Structural Biology Communications · OSTI ID:1625835

Schumacher, Maria A.; Ohashi, Tomoo; Corbin, Lauren; +1 more

A previously uncharacterized divisome-associated lipoprotein, DalA, is needed for normal cell division in Rhodobacterales

Journal Article · 2023 · mBio (Online) · OSTI ID:1987925

Alberge, François; Lakey, Bryan D.; Schaub, Ryan E.; +6 more

Cell Cycle-Dependent Recruitment of FtsN to the Divisome in Escherichia coli

Journal Article · 2022 · mBio (Online) · OSTI ID:1982980

Männik, Jaana; Pichoff, Sebastien; Lutkenhaus, Joe; +1 more

Title: Cell cycle‐dependent regulation of FtsZ in Escherichia coli in slow growth conditions

Citation Formats

References (63)

Similar Records

Related Subjects