1932

Abstract

How cells establish, maintain, and modulate size has always been an area of great interest and fascination. Until recently, technical limitations curtailed our ability to understand the molecular basis of bacterial cell size control. In the past decade, advances in microfluidics, imaging, and high-throughput single-cell analysis, however, have led to a flurry of work revealing size to be a highly complex trait involving the integration of three core aspects of bacterial physiology: metabolism, growth, and cell cycle progression.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090816-093803
2017-09-08
2024-12-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/71/1/annurev-micro-090816-093803.html?itemId=/content/journals/10.1146/annurev-micro-090816-093803&mimeType=html&fmt=ahah

Literature Cited

  1. Aarsman ME, Piette A, Fraipont C, Vinkenvleugel TM, Nguyen-Disteche M, den Blaauwen T. 1.  2005. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55:61631–45 [Google Scholar]
  2. Amelia M, Randich YVB. 2.  2015. Molecular mechanisms for the evolution of bacterial morphologies and growth modes. Front. Microbiol. 6:580 [Google Scholar]
  3. Amir A. 3.  2014. Cell size regulation in bacteria. Phys. Rev. Lett. 112:20208102 [Google Scholar]
  4. Amir A, Barkai N. 4.  2017. Is cell size a spandrel?. eLife 6:e22186 [Google Scholar]
  5. Arjes HA, Lai B, Emelue E, Steinbach A, Levin PA. 5.  2015. Mutations in the bacterial cell division protein FtsZ highlight the role of GTP binding and longitudinal subunit interactions in assembly and function. BMC Microbiol 15:1209 [Google Scholar]
  6. Bailey MW, Bisicchia P, Warren BT, Sherratt DJ, Männik J. 6.  2014. Evidence for divisome localization mechanisms independent of the Min system and SlmA in Escherichia coli. PLOS Genet. 10:8e1004504 [Google Scholar]
  7. Basan M, Zhu M, Dai X, Warren M, Sévin D. 7.  et al. 2015. Inflating bacterial cells by increased protein synthesis. Mol. Syst. Biol. 11:10836 [Google Scholar]
  8. Beaufay F, Coppine J, Mayard A, Laloux G, De Bolle X, Hallez R. 8.  2015. A NAD-dependent glutamate dehydrogenase coordinates metabolism with cell division in Caulobacter crescentus. EMBO J. 34:131786–800 [Google Scholar]
  9. Bisson-Filho A, Hsu YP, Squyres GR, Kuru E, Wu F. 9.  et al. 2017. Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division. Science 355:6326739–43 [Google Scholar]
  10. Bohin JP. 10.  2000. Osmoregulated periplasmic glucans in Proteobacteria. FEMS Microbiol. Lett. 186:111–19 [Google Scholar]
  11. Bohin JP, Kennedy EP. 11.  1984. Mapping of a locus (mdoA) that affects the biosynthesis of membrane-derived oligosaccharides in Escherichia coli. J. Bacteriol. 157:3956–57 [Google Scholar]
  12. Buddelmeijer N, Beckwith J. 12.  2004. A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol. Microbiol. 52:51315–27 [Google Scholar]
  13. Busiek KK, Eraso JM, Wang Y, Margolin W. 13.  2012. The early divisome protein FtsA interacts directly through its 1c subdomain with the cytoplasmic domain of the late divisome protein FtsN. J. Bacteriol. 194:81989–2000 [Google Scholar]
  14. Busiek KK, Margolin W. 14.  2014. A role for FtsA in SPOR-independent localization of the essential Escherichia coli cell division protein FtsN. Mol. Microbiol. 92:61212–26 [Google Scholar]
  15. Busiek KK, Margolin W. 15.  2015. Bacterial actin and tubulin homologs in cell growth and division. Curr. Biol. 25:6R243–54 [Google Scholar]
  16. Campos M, Surovtsev IV, Kato S, Paintdakhi A, Beltran B. 16.  et al. 2014. A constant size extension drives bacterial cell size homeostasis. Cell 159:61433–46 [Google Scholar]
  17. Chen JC, Beckwith J. 17.  2001. FtsQ, FtsL and FtsI require FtsK, but not FtsN, for co-localization with FtsZ during Escherichia coli cell division. Mol. Microbiol. 42:2395–413 [Google Scholar]
  18. Chien A-C, Zareh SKG, Wang YM, Levin PA. 18.  2012. Changes in the oligomerization potential of the division inhibitor UgtP co-ordinate Bacillus subtilis cell size with nutrient availability. Mol. Microbiol. 86:3594–610 [Google Scholar]
  19. Cho E, Ogasawara N, Ishikawa S. 19.  2008. The functional analysis of YabA, which interacts with DnaA and regulates initiation of chromosome replication in Bacillus subtilis. Genes Genet. Syst. 83:2111–25 [Google Scholar]
  20. Claessen D, Emmins R, Hamoen LW, Daniel RA, Errington J, Edwards DH. 20.  2008. Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Mol. Microbiol. 68:41029–46 [Google Scholar]
  21. Coltharp C, Buss J, Plumer TM, Xiao J. 21.  2016. Defining the rate-limiting processes of bacterial cytokinesis. PNAS 113:8E1044–53 [Google Scholar]
  22. Cooper S, Helmstetter CE. 22.  1968. Chromosome replication and the division cycle of Escherichia coli B/r. J. Mol. Biol. 31:3519–40 [Google Scholar]
  23. Dai K, Xu Y, Lutkenhaus J. 23.  1993. Cloning and characterization of ftsN, an essential cell division gene in Escherichia coli isolated as a multicopy suppressor of ftsA12(Ts). J. Bacteriol 175:123790–97 [Google Scholar]
  24. Daniel RA, Noirot-Gros MF, Noirot P, Errington J. 24.  2006. Multiple interactions between the transmembrane division proteins of Bacillus subtilis and the role of FtsL instability in divisome assembly. J. Bacteriol. 188:217396–404 [Google Scholar]
  25. de Boer PA, Crossley RE, Rothfield LI. 25.  1989. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56:4641–49 [Google Scholar]
  26. Domínguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Söldner R, Carballido-López R. 26.  2011. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:6039225–28 [Google Scholar]
  27. Donachie WD. 27.  1968. Relationship between cell size and time of initiation of DNA replication. Nature 219:51581077–79 [Google Scholar]
  28. Donachie WD, Blakely GW. 28.  2003. Coupling the initiation of chromosome replication to cell size in Escherichia coli. Curr. Opin. Microbiol. 6:2146–50 [Google Scholar]
  29. Dressaire C, Moreira RN, Barahona S, Alves de Matos AP, Arraiano CM. 29.  2015. BolA is a transcriptional switch that turns off motility and turns on biofilm development. mBio 6:1e02352–14 [Google Scholar]
  30. Du S, Pichoff S, Lutkenhaus J. 30.  2016. FtsEX acts on FtsA to regulate divisome assembly and activity. PNAS 113:34E5052–61 [Google Scholar]
  31. Duderstadt KE, Mott ML, Crisona NJ, Chuang K, Yang H, Berger JM. 31.  2010. Origin remodeling and opening in bacteria rely on distinct assembly states of the DnaA initiator. J. Biol. Chem. 285:3628229–39 [Google Scholar]
  32. Erzberger JP, Berger JM. 32.  2006. Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 35:93–114 [Google Scholar]
  33. Fenton AK, Gerdes K. 33.  2013. Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli. EMBO J 32:131953–65 [Google Scholar]
  34. Fernandez-Fernandez C, Gonzalez D, Collier J. 34.  2011. Regulation of the activity of the dual-function DnaA protein in Caulobacter crescentus. PLOS ONE 6:10e26028 [Google Scholar]
  35. Flåtten I, Fossum-Raunehaug S, Taipale R, Martinsen S, Skarstad K. 35.  2015. The DnaA protein is not the limiting factor for initiation of replication in Escherichia coli. PLOS Genet. 11:6e1005276 [Google Scholar]
  36. Fleurie A, Lesterlin C, Manuse S, Zhao C, Cluzel C. 36.  et al. 2014. MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae. Nature 516:7530259–62 [Google Scholar]
  37. Gamba P, Veening JW, Saunders NJ, Hamoen LW, Daniel RA. 37.  2009. Two-step assembly dynamics of the Bacillus subtilis divisome. J. Bacteriol. 191:134186–94 [Google Scholar]
  38. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T. 38.  2011. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333:6039222–25 [Google Scholar]
  39. Garrido T, Sánchez M, Palacios P, Aldea M, Vicente M. 39.  1993. Transcription of ftsZ oscillates during the cell cycle of Escherichia coli. EMBO J 12:103957–65 [Google Scholar]
  40. Geissler B, Shiomi D, Margolin W. 40.  2007. The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology 153:Pt. 3814–25 [Google Scholar]
  41. Gitai Z, Dye NA, Reisenauer A, Wachi M, Shapiro L. 41.  2005. MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120:329–41 [Google Scholar]
  42. Goranov AI, Breier AM, Merrikh H, Grossman AD. 42.  2009. YabA of Bacillus subtilis controls DnaA-mediated replication initiation but not the transcriptional response to replication stress. Mol. Microbiol. 74:2454–66 [Google Scholar]
  43. Haeusser DP, Garza AC, Buscher AZ, Levin PA. 43.  2007. The division inhibitor EzrA contains a seven-residue patch required for maintaining the dynamic nature of the medial FtsZ ring. J. Bacteriol. 189:249001–10 [Google Scholar]
  44. Haeusser DP, Margolin W. 44.  2016. Splitsville: structural and functional insights into the dynamic bacterial Z ring. Nat. Rev. Microbiol. 14:5305–19 [Google Scholar]
  45. Harris LK, Theriot JA. 45.  2016. Relative rates of surface and volume synthesis set bacterial cell size. Cell 165:61479–92 [Google Scholar]
  46. Harry EJ, Rodwell J, Wake RG. 46.  1999. Co-ordinating DNA replication with cell division in bacteria: a link between the early stages of a round of replication and mid-cell Z ring assembly. Mol. Microbiol. 33:133–40 [Google Scholar]
  47. Hill NS, Buske PJ, Shi Y, Levin PA. 47.  2013. A moonlighting enzyme links Escherichia coli cell size with central metabolism. PLOS Genet 9:7e1003663 [Google Scholar]
  48. Hill NS, Kadoya R, Chattoraj DK, Levin PA. 48.  2012. Cell size and the initiation of DNA replication in bacteria. PLOS Genet 8:3e1002549 [Google Scholar]
  49. Hirota Y, Ryter A, Jacob F. 49.  1968. Thermosensitive mutants of E. coli affected in the processes of DNA synthesis and cellular division. Cold Spring Harb. Symp. Quant. Biol. 33:0677–93 [Google Scholar]
  50. Iyer-Biswas S, Wright CS, Henry JT, Lo K, Burov S. 50.  et al. 2014. Scaling laws governing stochastic growth and division of single bacterial cells. PNAS 111:4515912–17 [Google Scholar]
  51. Jorasch P, Wolter FP, Zähringer U, Heinz E. 51.  1998. A UDP glucosyltransferase from Bacillus subtilis successively transfers up to four glucose residues to 1,2-diacylglycerol: expression of ypfP in Escherichia coli and structural analysis of its reaction products. Mol. Microbiol 29:2419–30 [Google Scholar]
  52. Jorgenson MA, Kannan S, Laubacher ME, Young KD. 52.  2015. Dead-end intermediates in the enterobacterial common antigen pathway induce morphological defects in Escherichia coli by competing for undecaprenyl phosphate. Mol. Microbiol. 100:11–14 [Google Scholar]
  53. Kaguni JM. 53.  2006. DnaA: controlling the initiation of bacterial DNA replication and more. Annu. Rev. Microbiol. 60:351–75 [Google Scholar]
  54. Katayama T, Ozaki S, Keyamura K, Fujimitsu K. 54.  2010. Regulation of the replication cycle: conserved and diverse regulatory systems for DnaA and oriC. Nat. Rev. Microbiol. 8:3163–70 [Google Scholar]
  55. Lange R, Hengge-Aronis R. 55.  1991. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S. J. Bacteriol 173:144474–81 [Google Scholar]
  56. Lazarevic V, Soldo B, Médico N, Pooley H, Bron S, Karamata D. 56.  2005. Bacillus subtilis alpha-phosphoglucomutase is required for normal cell morphology and biofilm formation. Appl. Environ. Microbiol. 71:139–45 [Google Scholar]
  57. Lenski RE, Travisano M. 57.  1994. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. PNAS 91:156808–14 [Google Scholar]
  58. Levin PA, Angert ER. 58.  2015. Small but mighty: cell size and bacteria. Cold Spring Harb. Perspect. Biol. 7:7a019216 [Google Scholar]
  59. Levin PA, Kurtser IG, Grossman AD. 59.  1999. Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. PNAS 96:179642–47 [Google Scholar]
  60. Levin PA, Schwartz RL, Grossman AD. 60.  2001. Polymer stability plays an important role in the positional regulation of FtsZ. J. Bacteriol. 183:185449–52 [Google Scholar]
  61. Levin S, Almo SC, Satir BH. 61.  1999. Functional diversity of the phosphoglucomutase superfamily: structural implications. Protein Eng 12:9737–46 [Google Scholar]
  62. Liu B, Persons L, Lee L, de Boer PAJ. 62.  2015. Roles for both FtsA and the FtsBLQ subcomplex in FtsN-stimulated cell constriction in Escherichia coli. Mol. Microbiol. 95:6945–70 [Google Scholar]
  63. Liu K, Bittner AN, Wang JD. 63.  2015. Diversity in (p)ppGpp metabolism and effectors. Curr. Opin. Microbiol. 24C:72–79 [Google Scholar]
  64. Løbner-Olesen A, Skarstad K, Hansen FG, von Meyenburg K, Boye E. 64.  1989. The DnaA protein determines the initiation mass of Escherichia coli K-12. Cell 57:5881–89 [Google Scholar]
  65. McCormick JR, Su EP, Driks A, Losick R. 65.  1994. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol. Microbiol 14:2243–54 [Google Scholar]
  66. Meeske AJ, Riley EP, Robins WP, Uehara T, Mekalanos JJ. 66.  et al. 2016. SEDS proteins are a widespread family of bacterial cell wall polymerases. Nature 537:7622634–38 [Google Scholar]
  67. Migocki MD, Freeman MK, Wake RG, Harry EJ. 67.  2002. The Min system is not required for precise placement of the midcell Z ring in Bacillus subtilis. EMBO Rep 3:121163–67 [Google Scholar]
  68. Modell JW, Kambara TK, Perchuk BS, Laub MT. 68.  2014. A DNA damage-induced, SOS-independent checkpoint regulates cell division in Caulobacter crescentus. PLOS Biol 12:10e1001977 [Google Scholar]
  69. Monahan LG, Hajduk IV, Blaber SP, Charles IG, Harry EJ. 69.  2014. Coordinating bacterial cell division with nutrient availability: a role for glycolysis. mBio 5:3e00935–14 [Google Scholar]
  70. Moriya S, Rashid RA, Rodrigues CDA, Harry EJ. 70.  2010. Influence of the nucleoid and the early stages of DNA replication on positioning the division site in Bacillus subtilis. Mol. Microbiol. 76:3634–47 [Google Scholar]
  71. Nishida S, Fujimitsu K, Sekimizu K, Ohmura T, Ueda T, Katayama T. 71.  2002. A nucleotide switch in the Escherichia coli DnaA protein initiates chromosomal replication: evidence from a mutant DnaA protein defective in regulatory ATP hydrolysis in vitro and in vivo. J. Biol. Chem. 277:1714986–95 [Google Scholar]
  72. Ogasawara N, Moriya S, Meyenburg von K, Hansen FG, Yoshikawa H. 72.  1985. Conservation of genes and their organization in the chromosomal replication origin region of Bacillus subtilis and Escherichia coli. EMBO J. 4:123345–50 [Google Scholar]
  73. Ogura Y, Imai Y, Ogasawara N, Moriya S. 73.  2001. Autoregulation of the dnaA-dnaN operon and effects of DnaA protein levels on replication initiation in Bacillus subtilis. J. Bacteriol. 183:133833–41 [Google Scholar]
  74. Ozaki S, Katayama T. 74.  2009. DnaA structure, function, and dynamics in the initiation at the chromosomal origin. Plasmid 62:271–82 [Google Scholar]
  75. Palacios P, Vicente M, Sánchez M. 75.  1996. Dependency of Escherichia coli cell-division size, and independency of nucleoid segregation on the mode and level of ftsZ expression. Mol. Microbiol. 20:51093–98 [Google Scholar]
  76. Pierucci O. 76.  1978. Dimensions of Escherichia coli at various growth rates: model for envelope growth. J. Bacteriol. 135:2559–74 [Google Scholar]
  77. Pogliano J, Pogliano K, Weiss DS, Losick R, Beckwith J. 77.  1997. Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites. PNAS 94:559–64 [Google Scholar]
  78. Powell BS, Court DL. 78.  1998. Control of ftsZ expression, cell division, and glutamine metabolism in Luria-Bertani medium by the alarmone ppGpp in Escherichia coli. J. Bacteriol. 180:51053–62 [Google Scholar]
  79. Pulschen AA, Sastre DE, Machinandiarena F, Crotta Asis A, Albanesi D. 79.  et al. 2016. The stringent response plays a key role in Bacillus subtilis survival of fatty acid starvation. Mol. Microbiol. 103:4698–712 [Google Scholar]
  80. Radhakrishnan SK, Pritchard S, Viollier PH. 80.  2010. Coupling prokaryotic cell fate and division control with a bifunctional and oscillating oxidoreductase homolog. Dev. Cell 18:190–101 [Google Scholar]
  81. Robson SA, Michie KA, Mackay JP, Harry E, King GF. 81.  2002. The Bacillus subtilis cell division proteins FtsL and DivIC are intrinsically unstable and do not interact with one another in the absence of other septasomal components. Mol. Microbiol. 44:3663–74 [Google Scholar]
  82. Rodrigues CDA, Harry EJ. 82.  2012. The Min system and nucleoid occlusion are not required for identifying the division site in Bacillus subtilis but ensure its efficient utilization. PLOS Genet 8:3e1002561 [Google Scholar]
  83. Santos JM, Lobo M, Matos APA, de Pedro MA, Arraiano CM. 83.  2002. The gene bolA regulates dacA (PBP5), dacC (PBP6) and ampC (AmpC), promoting normal morphology in Escherichia coli. Mol. Microbiol 45:61729–40 [Google Scholar]
  84. Sargent MG. 84.  1975. Control of cell length in Bacillus subtilis. J. Bacteriol. 123:17–19 [Google Scholar]
  85. Schaechter M, Maaløe O, Kjeldgaard NO. 85.  1958. Dependency on medium and temperature of cell size and chemical composition during balanced growth of Salmonella typhimurium. J. Gen. Microbiol. 19:3592–606 [Google Scholar]
  86. Schreiber G, Ron EZ, Glaser G. 86.  1995. ppGpp-mediated regulation of DNA replication and cell division in Escherichia coli. Curr. Microbiol. 30:127–32 [Google Scholar]
  87. Seyfzadeh M, Keener J, Nomura M. 87.  1993. SpoT-dependent accumulation of guanosine tetraphosphate in response to fatty acid starvation in Escherichia coli. PNAS 90:2311004–8 [Google Scholar]
  88. Si F, Li D, Cox SE, Sauls JT, Azizi O. 88.  et al. 2017. Invariance of initiation mass and predictability of cell size in Escherichia coli. Curr. Biol. 27:81278–87 [Google Scholar]
  89. Stott KV, Wood SM, Blair JA, Nguyen BT, Herrera A. 89.  et al. 2015. (p)ppGpp modulates cell size and the initiation of DNA replication in Caulobacter crescentus in response to a block in lipid biosynthesis. Microbiology 161:Pt. 3553–64 [Google Scholar]
  90. Taheri-Araghi S, Bradde S, Sauls JT, Hill NS, Levin PA. 90.  et al. 2015. Cell-Size control and homeostasis in bacteria. Curr. Biol. 25:3385–91 [Google Scholar]
  91. Tanouchi Y, Pai A, Park H, Huang S, Stamatov R. 91.  et al. 2015. A noisy linear map underlies oscillations in cell size and gene expression in bacteria. Nature 523:7560357–60 [Google Scholar]
  92. Tedin K, Bremer H. 92.  1992. Toxic effects of high levels of ppGpp in Escherichia coli are relieved by rpoB mutations. J. Biol. Chem 267:42337–44 [Google Scholar]
  93. Tehranchi AK, Blankschien MD, Zhang Y, Halliday JA, Srivatsan A. 93.  et al. 2010. The transcription factor DksA prevents conflicts between DNA replication and transcription machinery. Cell 141:4595–605 [Google Scholar]
  94. Treuner-Lange A, Aguiluz K, van der Does C, Gómez-Santos N, Harms A. 94.  et al. 2013. PomZ, a ParA-like protein, regulates Z-ring formation and cell division in Myxococcusxanthus. Mol. Microbiol. 87:2235–53 [Google Scholar]
  95. Tropini C, Lee TK, Hsin J, Desmarais SM, Ursell T. 95.  et al. 2014. Principles of bacterial cell-size determination revealed by cell-wall synthesis perturbations. Cell Rep 9:41520–27 [Google Scholar]
  96. Tsang M-J, Bernhardt TG. 96.  2015. A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division. Mol. Microbiol. 95:6925–44 [Google Scholar]
  97. Vadia S, Tse JL, Lucena R, Yang Z, Kellogg DR. 97.  et al. 2017. Fatty acid availability sets cell envelope capacity and dictates microbial cell size. Curr. Biol. 27:121757–67 [Google Scholar]
  98. Varma A, de Pedro MA, Young KD. 98.  2007. FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli.. J. Bacteriol. 189:155692–704 [Google Scholar]
  99. Varma A, Young KD. 99.  2009. In Escherichia coli, MreB and FtsZ direct the synthesis of lateral cell wall via independent pathways that require PBP 2. J. Bacteriol. 191:113526–33 [Google Scholar]
  100. Wallden M, Fange D, Lundius EG, Baltekin Ö, Elf J. 100.  2016. The synchronization of replication and division cycles in individual E.coli cells. Cell 166:3729–39 [Google Scholar]
  101. Wang L, Khattar MK, Donachie WD, Lutkenhaus J. 101.  1998. FtsI and FtsW are localized to the septum in Escherichia coli.. J. Bacteriol. 180:112810–16 [Google Scholar]
  102. Weart RB, Lee AH, Chien A-C, Haeusser DP, Hill NS, Levin PA. 102.  2007. A metabolic sensor governing cell size in bacteria. Cell 130:2335–47 [Google Scholar]
  103. Weart RB, Levin PA. 103.  2003. Growth rate-dependent regulation of medial FtsZ ring formation. J. Bacteriol. 185:92826–34 [Google Scholar]
  104. Wientjes FB, Nanninga N. 104.  1989. Rate and topography of peptidoglycan synthesis during cell division in Escherichia coli: concept of a leading edge. J. Bacteriol. 171:63412–19 [Google Scholar]
  105. Willemse J, Borst JW, de Waal E, Bisseling T, van Wezel GP. 105.  2011. Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev 25:189–99 [Google Scholar]
  106. Woldringh CL, Huls P, Pas E, Brakenhoff GJ, Nanninga N. 106.  1987. Topography of peptidoglycan synthesis during elongation and polar cap formation in a cell division mutant of Escherichia coli MC4100. Microbiology 133:3575–86 [Google Scholar]
  107. Yang X, Lyu Z, Miguel A, McQuillen R, Huang KC, Xiao J. 107.  2017. GTPase activity-coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis. Science 355:6326744–47 [Google Scholar]
  108. Yao Z, Davis RM, Kishony R, Kahne D, Ruiz N. 108.  2012. Regulation of cell size in response to nutrient availability by fatty acid biosynthesis in Escherichia coli. PNAS 109:38E2561–68 [Google Scholar]
  109. Young KD. 109.  2010. Bacterial shape: two-dimensional questions and possibilities. Annu. Rev. Microbiol. 64:1223–40 [Google Scholar]
  110. Yu X-C, Margolin W. 110.  1999. FtsZ ring clusters in min and partition mutants: role of both the Min system and the nucleoid in regulating FtsZ ring localization. Mol. Microbiol. 32:2315–26 [Google Scholar]
  111. Zheng H, Ho P-Y, Jiang M, Bin Tang, Liu W. 111.  et al. 2016. Interrogating the Escherichia coli cell cycle by cell dimension perturbations. PNAS 113:5215000–5 [Google Scholar]
/content/journals/10.1146/annurev-micro-090816-093803
Loading
/content/journals/10.1146/annurev-micro-090816-093803
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error