Splitsville: Structural and functional insights into the dynamic bacterial Z ring

Nature Reviews Microbiology

Volumn 14, Issue 5, 2016, Pages 305-319

  Haeusser, Daniel P ^a,b   Margolin, William ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b CANISIUS COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; FTSZ PROTEIN; BACTERIAL PROTEIN; CYTOSKELETON PROTEIN; FTSZ PROTEIN, BACTERIA;

BACTERIAL CELL; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIUM; CELL DIVISION; CYTOKINESIS; MATURATION; MECHANICAL STRESS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; CELL CYCLE; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; ULTRASTRUCTURE;

BACTERIA; BACTERIAL PROTEINS; CELL CYCLE; CELL MEMBRANE; CYTOKINESIS; CYTOSKELETAL PROTEINS;

EID: 84962069677     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro.2016.26     Document Type: Review

References (156)

1. Egan, A. J., & Vollmer, W. The physiology of bacterial cell division. Ann. NY Acad. Sci. 1277, 8-28 (2013
2. Brown P. J., et al. Polar growth in the alphaproteobacterial order Rhizobiales. Proc. Natl Acad. Sci. USA 109, 1697-1701 (2011
3. Margolin, W. Themes and variations in prokaryotic cell division. FEMS Microbiol. Rev. 24, 531-548 (2000
4. Leisch N., et al. Growth in width and FtsZ ring longitudinal positioning in a gammaproteobacterial symbiont. Curr. Biol. 22, R831-R832 (2012
5. Monahan, L. G., Liew, A. T., Bottomley, A. L., & Harry, E. J. Division site positioning in bacteria: one size does not fit all. Front. Microbiol. 5, 19 (2014
6. Rowlett, V. W., & Margolin, W. The Min system and other nucleoid-independent regulators of Z ring positioning. Front. Microbiol. 6, 478 (2015
7. Willemse, J., Borst, J. W., de Waal, E., Bisseling, T., & van Wezel, G. P. Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev. 25, 89-99 (2011
8. Treuner-Lange, A., et al. PomZ, a ParA-like protein, regulates Z ring formation and cell division in Myxococcus xanthus. Mol. Microbiol. 87, 235-253 (2013
9. Holeckova N., et al. LocZ is a new cell division protein involved in proper septum placement in Streptococcus Pneumoniae. mBio 6, e01700 14 (2014
10. Fleurie A., et al. MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae. Nature 516, 259-262 (2014
11. McCormick, J. R., Su, E. P., Driks, A., & Losick, R. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol. 14, 243-254 (1994
12. Rico, A. I., Krupka, M., & Vicente, M. In the beginning. Escherichia coli assembled the proto-ring: an initial phase of division. J. Biol. Chem. 288, 20830-20836 (2013
13. Pichoff, S., & Lutkenhaus, J. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55, 1722-1734 (2005
14. Hale, C. A., & de Boer, P. A. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88, 175-185 (1997
15. Pichoff, S., & Lutkenhaus, J. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21, 685-693 (2002
16. Duman R., et al. Structural and genetic analyses reveal the protein SepF as a new membrane anchor for the Z ring. Proc. Natl Acad. Sci. USA 110, E4601-E4610 (2013
17. Krol E., et al. Bacillus subtilis SepF binds to the C terminus of FtsZ. PLoS ONE 7, e43293 (2013
18. Ishikawa, S., Kawai, Y., Hiramatsu, K., Kuwano, M., & Ogasawara, N. A new FtsZ-interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis. Mol. Microbiol. 60, 1364-1380 (2006
19. Gupta S., et al. The essential protein SepF of mycobacteria interacts with FtsZ and MurG to regulate cell growth and division. Microbiology 161, 1627-1638 (2015
20. Gola, S., Munder, T., Casonato, S., Manganelli, R., & Vicente, M. The essential role of SepF in mycobacterial division. Mol. Microbiol. 97, 560-576 (2015
21. Levin, P. A., Kurtser, I. G., & Grossman, A. D. Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc. Natl Acad. Sci. USA 96, 9642-9647 (1999
22. Steele, V. R., Bottomley, A. L., Garcia-Lara, J., Kasturiarachchi, J., & Foster, S. J. Multiple essential roles for EzrA in cell division of Staphylococcus aureus. Mol. Microbiol. 80, 542-555 (2011
23. Haeusser D. P., et al. EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol. Microbiol. 52, 801-814 (2004
24. Cleverley R. M., et al. Structure and function of a spectrin-like regulator of bacterial cytokinesis. Nat. Commun. 5, 5421 (2014
25. Machnicka, B., et al. Spectrins: a structural platform for stabilization and activation of membrane channels, receptors and transporters. Biochim. Biophys. Acta 1838, 620-634 (2014
26. Haeusser, D. P., Garza, A. C., Buscher, A. Z., & Levin, P. A. The division inhibitor EzrA contains a seven-residue patch required for maintaining the dynamic nature of the medial FtsZ ring. J. Bacteriol. 189, 9001-9010 (2007
27. Land, A. D., Luo, Q., & Levin, P. A. Functional domain analysis of the cell division inhibitor EzrA. PLoS ONE 9, e102616 (2014
28. Son, S. H., & Lee, H. H. The N terminal domain of EzrA binds to the C terminus of FtsZ to inhibit Staphylococcus aureus FtsZ polymerization. Biochem. Biophys. Res. Commun. 433, 108-114 (2013
29. van den Ent, F., & Löwe, J. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J. 19, 5300-5307 (2000
30. Sanchez, M., Valencia, A., Ferrandiz, M. J., Sandler, C., & Vicente, M. Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family. EMBO J. 13, 4919-4925 (1994
31. Feucht, A., Lucet, I., Yudkin, M. D., & Errington, J. Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis. Mol. Microbiol. 40, 115-125 (2001
32. Paradis-Bleau, C., Sanschagrin, F., & Levesque, R. C. Peptide inhibitors of the essential cell division protein FtsA. Protein Eng. Des. Sel. 18, 85-91 (2005
33. Lara B., et al. Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol. Microbiol. 55, 699-711 (2005
34. Szwedziak, P., Wang, Q., Freund, S. M., & Löwe, J. FtsA forms actin-like protofilaments. EMBO J. 31, 2249-2260 (2012
35. Pichoff, S., Shen, B., Sullivan, B., & Lutkenhaus, J. FtsA mutants impaired for self-interaction bypass ZipA suggesting a model in which FtsA?s self-interaction competes with its ability to recruit downstream division proteins. Mol. Microbiol. 83, 151-167 (2012
36. Shiomi, D., & Margolin, W. Dimerization or oligomerization of the actin-like FtsA protein enhances the integrity of the cytokinetic Z ring. Mol. Microbiol. 66, 1396-1415 (2007
37. Fujita J., et al. Crystal structure of FtsA from Staphylococcus aureus. FEBS Lett. 588, 1879-1885 (2014
38. Geissler, B., Elraheb, D., & Margolin, W. A gain of function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli. Proc. Natl Acad. Sci. USA 100, 4197-4202 (2003
39. Geissler, B., & Margolin, W. Evidence for functional overlap among multiple bacterial cell division proteins: compensating for the loss of FtsK. Mol. Microbiol. 58, 596-612 (2005
40. Beuria T. K., et al. Adenine nucleotide-dependent regulation of assembly of bacterial tubulin-like FtsZ by a hypermorph of bacterial actin-like FtsA. J. Biol. Chem. 284, 14079-14086 (2009
41. Loose, M., & Mitchison, T. J. The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat. Cell Biol. 16, 38-46 (2014
42. Modi, K., & Misra, H. S. Dr FtsA, an actin homologue in Deinococcus radiodurans differentially affects Dr FtsZ and Ec FtsZ functions in vitro. PLoS ONE 9, e115918 (2014
43. Du, S., Park, K. T., & Lutkenhaus, J. Oligomerization of FtsZ converts the FtsZ tail motif (CCTP) into a multivalent ligand with high avidity for partners ZipA and SlmA. Mol. Microbiol. 95, 173-188 (2015
44. Herricks, J. R., Nguyen, D., & Margolin, W. A thermosensitive defect in the ATP binding pocket of FtsA can be suppressed by allosteric changes in the dimer interface. Mol. Microbiol. 94, 713-727 (2014
45. Shen, B., & Lutkenhaus, J. The conserved C terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinCC/MinD. Mol. Microbiol. 72, 410-424 (2009
46. Rowlett, V. W., & Margolin, W. Asymmetric constriction of dividing Escherichia coli cells induced by expression of a fusion between two Min proteins. J. Bacteriol. 196, 2089-2100 (2014
47. Szwedziak, P., Wang, Q., Bharat, T. A. M., Tsim, M., & Löwe, J. Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. eLife 3, e04601 (2014
48. Hernandez-Rocamora V. M., et al. Dynamic interaction of the Escherichia coli cell division ZipA and FtsZ proteins evidenced in nanodiscs. J. Biol. Chem. 287, 30097-30104 (2012
49. Skoog, K., & Daley, D. O. The Escherichia coli cell division protein ZipA forms homodimers prior to association with FtsZ. Biochemistry 51, 1407-1415 (2012
50. Jaiswal, R., et al. E93R substitution of Escherichia coli FtsZ induces bundling of protofilaments, reduces GTPase activity, and impairs bacterial cytokinesis. J. Biol. Chem. 285, 31796-31805 (2010
51. Haeusser, D. P., Rowlett, V. W., & Margolin, W. A mutation in Escherichia coli ftsZ bypasses the requirement for the essential division gene zipA and confers resistance to FtsZ assembly inhibitors by stabilizing protofilament bundling. Mol. Microbiol. 97, 988-1005 (2015
52. Dewar, S. J., Begg, K. J., & Donachie, W. D. Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J. Bacteriol. 174, 6314-6316 (1992
53. Mukherjee, A., & Lutkenhaus, J. Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J. 17, 462-469 (1998
54. Scheffers, D. J., de Wit, J. G., den Blaauwen, T., & Driessen, A. J. GTP hydrolysis of cell division protein FtsZ: evidence that the active site is formed by the association of monomers. Biochemistry 41, 521-529 (2002
55. Huang, K. H., Durand-Heredia, J., & Janakiraman, A. FtsZ ring stability: of bundles, tubules, crosslinks, and curves. J. Bacteriol. 195, 1859-1868 (2013
56. Meier, E. L., & Goley, E. D. Form and function of the bacterial cytokinetic ring. Curr. Opin. Cell Biol. 26, 147 (2014
57. Rowlett, V. W., & Margolin, W. The bacterial divisome: ready for its close up. Phil. Trans. R. Soc. Lond. B Biol. Sci. 370, 20150028 (2015
58. Li, Z., Trimble, M. J., Brun, Y. V., & Jensen, G. J. The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J. 26, 4694-4708 (2007
59. Holden S. J., et al. High throughput 3D super-resolution microscopy reveals Caulobacter crescentus in vivo Z ring organization. Proc. Natl Acad. Sci. USA 111, 4566-4571 (2014
60. Jacq M., et al. Remodeling of the Z ring nanostructure during the Streptococcus pneumoniae cell cycle revealed by photoactivated localization microscopy. mBio 6, e01108 15 (2015
61. Strauss, M. P., et al. 3D SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol. 10 e1001389 2012
62. Rowlett, V. W., & Margolin, W. 3D SIM super-resolution of FtsZ and its membrane tethers in Escherichia coli cells. Biophys. J. 107, L17-L20 (2014
63. Tsui H. C. T., et al. Pbp2x localizes separately from Pbp2b and other peptidoglycan synthesis proteins during later stages of cell division of Streptococcus pneumoniae D39. Mol. Microbiol. 94, 21-40 (2014
64. Piro, O., Carmon, G., Feingold, M., & Fishov, I. Three-dimensional structure of the Z ring as a random network of FtsZ filaments. Env. Microbiol. 15, 3252-3258 (2013
65. Si, F., Busiek, K., Margolin, W., & Sun, S. X. Organization of FtsZ filaments in the bacterial division ring measured from polarized fluorescence microscopy. Biophys. J. 105, 1976-1986 (2013
66. Judd, E. M., et al. Distinct constrictive processes, separated in time and space, divide Caulobacter inner and outer membranes. J. Bacteriol. 187, 6874-6882 (2005
67. Gundogdu M. E., et al. Large ring polymers align FtsZ polymers for normal septum formation. EMBO J. 30, 617-626 (2011
68. Hale, C. A., Rhee, A. C., & de Boer, P. A. ZipA-induced bundling of FtsZ polymers mediated by an interaction between C terminal domains. J. Bacteriol. 182, 5153-5166 (2000
69. Roach, E. J., Kimber, M. S., & Khursigara, C. M. Crystal structure and site-directed mutational analysis reveals key residues involved in Escherichia coli ZapA function. J. Biol. Chem. 289, 23276-23286 (2014
70. Durand-Heredia, J. M., Yu, H. H., De Carlo, S., Lesser, C. F., & Janakiraman, A. Identification and characterization of ZapC, a stabilizer of the FtsZ ring in Escherichia coli. J. Bacteriol. 193, 1405-1413 (2011
71. Hale C. A., et al. Identification of Escherichia coli ZapC (YcbW) as a component of the division apparatus that binds and bundles FtsZ polymers. J. Bacteriol. 193, 1393-1404 (2011
72. Durand-Heredia, J., Rivkin, E., Fan, G., Morales, J., & Janakiraman, A. Identification of ZapD as a cell division factor that promotes the assembly of FtsZ in Escherichia coli. J. Bacteriol. 194, 3189-3198 (2012
73. Buss J., et al. In vivo organization of the FtsZ-ring by ZapA and ZapB revealed by quantitative super-resolution microscopy. Mol. Microbiol. 89, 1099-1120 (2013
74. Gardner, K. A., Moore, D. A., & Erickson, H. P. The C terminal linker of Escherichia coli FtsZ functions as an intrinsically disordered peptide. Mol. Microbiol. 89, 264-275 (2013
75. Buske, P. J., & Levin, P. A. A flexible C terminal linker is required for proper FtsZ assembly in vitro and cytokinetic ring formation in vivo. Mol. Microbiol. 89, 249-263 (2013
76. Sundararajan K., et al. The bacterial tubulin FtsZ requires its intrinsically disordered linker to direct robust cell wall construction. Nat. Commun. 6, 7281 (2015
77. Buske, P. J., & Levin, P. A. Extreme C-Terminus of bacterial cytoskeletal protein FtsZ plays fundamental role in assembly independent of modulatory proteins. J. Biol. Chem. 287, 10945-10957 (2012
78. Fu G., et al. in vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS ONE 5, e12682 (2010
79. Aarsman M. E., et al. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55, 1631-1645 (2005
80. Gamba, P., Veening, J. W., Saunders, N. J., Hamoen, L. W., & Daniel, R. A. Two-step assembly dynamics of the Bacillus subtilis divisome. J. Bacteriol. 191, 4186-4194 (2009
81. Mohammadi T., et al. Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J. 30, 1425-1432 (2011
82. Sham L. T., et al. Bacterial cell wall. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345, 220-222 (2014
83. Van den Berg van Saparoea H. B., et al. Fine-mapping the contact sites of the Escherichia coli cell division proteins FtsB and FtsL on the FtsQ protein. J. Biol. Chem. 288, 24340-24350 (2013
84. Khadria, A. S., & Senes, A. The transmembrane domains of the bacterial cell division proteins FtsB and FtsL form a stable high-order oligomer. Biochemistry 52, 7542-7550 (2013
85. Glas M., et al. The soluble periplasmic domains of E. coli cell division proteins FtsQ/FtsB/FtsL form a trimeric complex with sub-micromolar affinity. J. Biol. Chem. 290, 21498-21509 (2015
86. Bottomley A. L., et al. Staphylococcus aureus DivIB is a peptidoglycan-binding protein that is required for a morphological checkpoint in cell division. Mol. Microbiol. 94, 1041-1064 (2014
87. Grenga, L., Rizzo, A., Paolozzi, L., & Ghelardini, P. Essential and non-essential interactions in interactome networks: the Escherichia coli division proteins FtsQ-FtsN interaction. Env. Microbiol. 15, 3210-3217 (2013
88. Alexeeva S., et al. Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol. Microbiol. 77, 384-398 (2010
89. Busiek, K. K., Eraso, J. M., Wang, Y., & Margolin, W. The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J. Bacteriol. 194, 1989-2000 (2012
90. Rico, A. I., Garcia-Ovalle, M., Mingorance, J., & Vicente, M. Role of two essential domains of Escherichia coli FtsA in localization and progression of the division ring. Mol. Microbiol. 53, 1359-1371 (2004
91. Yahashiri, A., Jorgenson, M. A., & Weiss, D. S. Bacterial SPOR domains are recruited to septal peptidoglycan by binding to glycan strands that lack stem peptides. Proc. Natl Acad. Sci. USA 112, 11347-11352 (2015
92. Gerding, M. A., et al. Self-enhanced accumulation of FtsN at division sites and roles for other proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction. J. Bacteriol. 191, 7383-7401 (2009
93. Busiek, K. K., & Margolin, W. A role for FtsA in SPOR-independent localization of the essential Escherichia coli cell division protein FtsN. Mol. Microbiol. 92, 1212-1226 (2014
94. Bernard, C. S., Sadasivam, M., Shiomi, D., & Margolin, W. An altered FtsA can compensate for the loss of essential cell division protein FtsN in Escherichia coli. Mol. Microbiol. 64, 1289-1305 (2007
95. Liu, B., Persons, L., Lee, L., & de Boer, P. Roles for both FtsA and the FtsBLQ subcomplex in FtsN-stimulated cell constriction in Escherichia coli. Mol. Microbiol. 95, 945-970 (2015
96. Pichoff, S., Du, S., & Lutkenhaus, J. The bypass of ZipA by overexpression of FtsN requires a previously unknown conserved FtsN motif essential for FtsA-FtsN interaction supporting a model in which FtsA monomers recruit late cell division proteins to the Z ring. Mol. Microbiol. 95, 971-987 (2015
97. Tsang, M. J., & Bernhardt, T. G. A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division. Mol. Microbiol. 95, 925-944 (2015
98. Potluri, L. P., Kannan, S., & Young, K. D. ZipA is required for FtsZ-dependent preseptal peptidoglycan synthesis prior to invagination during cell division. J. Bacteriol. 194, 5334-5342 (2012
99. Claessen D., et al. Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Mol. Microbiol. 68, 1029-1046 (2008
100. Land A. D., et al. Requirement of essential Pbp2x and GpsB for septal ring closure in Streptococcus pneumoniae D39. Mol. Microbiol. 90, 939-955 (2013
101. Fleurie A., et al. Interplay of the serine/threonine-kinase StkP and the paralogs DivIVA and GpsB in pneumococcal cell elongation and division. PLoS Genet. 10, e1004275 (2014
102. Pompeo, F., Foulquier, E., Serrano, B., Grangeasse, C., & Galinier, A. Phosphorylation of the cell division protein GpsB regulates PrkC kinase activity through a negative feedback loop in Bacillus subtilis. Mol. Microbiol. 97, 139-150 (2015
103. Gerding, M. A., Ogata, Y., Pecora, N. D., Niki, H., & de Boer, P. A. The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol. Microbiol. 63, 1008-1025 (2007
104. Gray A. N., et al. Coordination of peptidoglycan synthesis and outer membrane constriction during Escherichia coli cell division. eLife 4, e07118 (2015
105. Corbin, B. D., Wang, Y., Beuria, T. K., & Margolin, W. Interaction between cell division proteins FtsE and FtsZ. J. Bacteriol. 189, 3026-3035 (2007
106. Yang D. C., et al. An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring. Proc. Natl Acad. Sci. USA 108, E1052-E1060 (2011
107. Jorgenson, M. A., Chen, Y., Yahashiri, A., Popham, D. L., & Weiss, D. S. The bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod shape and daughter cell separation in Pseudomonas aeruginosa. Mol. Microbiol. 93, 113-128 (2014
108. Osawa, M., Anderson, D. E., & Erickson, H. P. Reconstitution of contractile FtsZ rings in liposomes. Science 320, 792-794 (2008
109. Osawa, M., & Erickson, H. P. Liposome division by a simple bacterial division machinery. Proc. Natl Acad. Sci. USA 110, 11000-11004 (2013
110. Dow, C. E., van den Berg, H. A., Roper, D. I., & Rodger, A. Biological insights from a simulation model of the critical FtsZ accumulation required for prokaryotic cell division. Biochemistry 54, 3803-3813 (2015
111. Li Y., et al. FtsZ protofilaments use a hinge-opening mechanism for constrictive force generation. Science 341, 392-395 (2013
112. Söderström B., et al. Disassembly of the divisome in Escherichia coli: evidence that FtsZ dissociates before compartmentalization. Mol. Microbiol. 92, 1-9 (2014
113. Krupka M., et al. Role of the FtsA C-Terminus as a switch for polymerization and membrane association. mBio 5, e02221 (2014
114. Cabre E. J., et al. Bacterial division proteins FtsZ and ZipA induce vesicle shrinkage and cell membrane invagination. J. Biol. Chem. 288, 26625-26634 (2013
115. Weiss D. S. Last but not least: new insights into how FtsN triggers constriction during Escherichia coli cell division. Mol. Microbiol. 903-909 2015
116. Tsang, M. J., & Bernhardt, T. G. Guiding divisome assembly and controlling its activity. Curr. Opin. Microbiol. 24, 60-65 (2015
117. Weart, R B., et al. A metabolic sensor governing cell size in bacteria. Cell 130 335-347 2007
118. Chien, A. C., Zareh, S. K., Wang, Y. M., & Levin, P. A. Changes in the oligomerization potential of the division inhibitor UgtP co ordinate Bacillus subtilis cell size with nutrient availability. Mol. Microbiol. 86, 594-610 (2012
119. Hill, N. S., Buske, P. J., Shi, Y., & Levin, P. A. A moonlighting enzyme links Escherichia coli cell size with central metabolism. PLoS Genet. 9 e1003663 2013
120. Surdova K., et al. The conserved DNA-binding protein WhiA is involved in cell division in Bacillus subtilis. J. Bacteriol. 195, 5450-5460 (2013
121. Monahan, L. G., Hajduk, I. V., Blaber, S. P., Charles, I. G., & Harry, E. J. Coordinating bacterial cell division with nutrient availability: a role for glycolysis. mBio 5, e00935 14 (2014
122. Radhakrishnan, S. K., Pritchard, S., & Viollier, P. H. Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog. Dev. Cell 18, 90-101 (2010
123. Beaufay F. et al. A NAD-dependent glutamate dehydrogenase coordinates metabolism with cell division in Caulobacter crescentus. EMBO J. 34, 1786-1800 2015
124. Takada H., et al. An essential enzyme for phospholipid synthesis associates with the Bacillus subtilis divisome. Mol. Microbiol. 91, 242-255 (2014
125. Weart, R. B., Nakano, S., Lane, B. E., Zuber, P., & Levin, P. A. The ClpX chaperone modulates assembly of the tubulin-like protein FtsZ. Mol. Microbiol. 57, 238-249 (2005
126. Camberg, J. L., Hoskins, J. R., & Wickner, S. The interplay of ClpXP with the cell division machinery in Escherichia coli. J. Bacteriol. 193, 1911-1918 (2011
127. Williams, B., Bhat, N., Chien, P., & Shapiro, L. ClpXP and ClpAP proteolytic activity on divisome substrates is differentially regulated following the Caulobacter asymmetric cell division. Mol. Microbiol. 93, 853-866 (2014
128. Chen, Y., Milam, S. L., & Erickson, H. P. SulA inhibits assembly of FtsZ by a simple sequestration mechanism. Biochemistry 51, 3100-3109 (2012
129. Modell, J. W., Hopkins, A. C., & Laub, M. T. DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW. Genes Dev. 25, 1328-1343 (2011
130. Modell, J. W., Kambara, T. K., Perchuk, B. S., & Laub, M. T. DNA damage-induced, SOS-independent checkpoint regulates cell division in Caulobacter crescentus. PLoS Biol. 12, e1001977 (2014
131. Mo, A. H., & Burkholder, W. F. YneA, an SOS-induced inhibitor of cell division in Bacillus subtilis, is regulated posttranslationally and requires the transmembrane region for activity. J. Bacteriol. 192, 3159-3173 (2010
132. Buchholz, M., Nahrstedt, H., Pillukat, M. H., Deppe, V., & Meinhardt, F. yneA mRNA instability is involved in temporary inhibition of cell division during the SOS response of Bacillus megaterium. Microbiology 159, 1564-1574 (2013
133. Marteyn B. S., et al. ZapE is a novel cell division protein interacting with FtsZ and modulating the Z ring dynamics. mBio 5, e00022 14 (2014
134. Koprowski P., et al. Cytoplasmic domain of MscS interacts with cell division protein FtsZ: A possible non-channel function of the mechanosensitive channel in Escherichia coli. PLoS ONE 10, e0127029 (2015
135. Wilson, M. E., Jensen, G. S., & Haswell, E. S. Two mechanosensitive channel homologs influence division ring placement in Arabidopsis chloroplasts. Plant Cell 23, 2939-2949 (2011
136. Mercier, R., Kawai, Y., & Errington, J. General principles for the formation and proliferation of a wall-free (L form) state in bacteria. eLife 3, e04629 (2014
137. Lock, R. L., & Harry, E. J. Cell-division inhibitors: new insights for future antibiotics. Nat. Rev. Drug Discov. 7, 324-338 (2008
138. Ojima, I., Kumar, K., Awasthi, D., & Vineberg, J. G. Drug discovery targeting cell division proteins, microtubules and FtsZ. Bioorg. Med. Chem. 22, 5060-5077 (2014
139. Sass, P., & Brotz-Oesterhelt, H. Bacterial cell division as a target for new antibiotics. Curr. Opin. Microbiol. 16, 522-530 (2013
140. Artola M., et al. Effective GTP-replacing FtsZ inhibitors and antibacterial mechanism of action. ACS Chem. Biol. 10, 834-843 (2014
141. Haeusser D. P., et al. The Kil peptide of bacteriophage γ blocks Escherichia coli cytokinesis via ZipA-dependent inhibition of FtsZ assembly. PLoS Genet. 10, e1004217 (2014
142. Kiro R., et al. Gene product 0.4 increases bacteriophage T7 competitiveness by inhibiting host cell division. Proc. Natl Acad. Sci. USA 110, 19549-19554 (2013
143. Hernandez-Rocamora, V. M., Alfonso, C., Margolin, W., Zorrilla, S., & Rivas, G. Evidence that bacteriophage γ Kil peptide inhibits bacterial cell division by disrupting FtsZ protofilaments and sequestering protein subunits. J. Biol. Chem. 290, 20325-20335 (2015
144. Ballesteros-Plaza, D., Holguera, I., Scheffers, D. J., Salas, M., & Munoz-Espin, D. Phage φ29 protein p1 promotes replication by associating with the FtsZ ring of the divisome in Bacillus subtilis. Proc. Natl Acad. Sci. USA 110, 12313-12318 (2013
145. Bisson-Filho, A. W., et al. FtsZ filament capping by MciZ, a developmental regulator of bacterial division. Proc. Natl Acad. Sci. USA 112, E2130-E2138 (2015
146. Pende N., et al. Size-independent symmetric division in extraordinarily long cells. Nat. Commun. 5, 4803 (2014
147. Donovan, C., & Bramkamp, M. Cell division in Corynebacterineae. Front. Microbiol. 5, 132 (2014
148. Kieser, K. J., & Rubin, E. J. How sisters grow apart: mycobacterial growth and division. Nat. Rev. Microbiol. 12, 550-562 (2014
149. Ramos-Leon, F., Mariscal, V., Frias, J. E., Flores, E., & Herrero, A. Divisome-dependent subcellular localization of cell-cell joining protein SepJ in the filamentous cyanobacterium Anabaena. Mol. Microbiol. 96, 566-580 (2015
150. Pinho, M. G., Kjos, M., & Veening, J. W. How to get (a) round: mechanisms controlling growth and division of coccoid bacteria. Nat. Rev. Microbiol. 11, 601-614 (2013
151. Angert, E. R. Alternatives to binary fission in bacteria. Nat. Rev. Microbiol. 3, 214-224 (2005
152. Tuson, H. H., & Biteen, J. S. Unveiling the inner workings of live bacteria using super-resolution microscopy. Anal. Chem. 87, 42-63 (2015
153. Asano, S., Engel, B. D., & Baumeister, W. In situ cryo-electron tomography: A post-reductionist approach to structural biology. J. Mol. Biol. 428, 332-343 (2015
154. Busiek, K. K., & Margolin, W. Bacterial actin and tubulin homologs in cell growth and division. Curr. Biol. 25, 245-254 (2015
155. Grainge, I. FtsK-A bacterial cell division checkpoint?. Mol. Microbiol. 78, 1055-1057 (2010
156. Buss, J., et al. A multi-layered protein network stabilizes the Escherichia coli FtsZ-ring and modulates constriction dynamics. PLoS Genet. 11 e1005128 2015