Defining the rate-limiting processes of bacterial cytokinesis

被引:106
作者
Coltharp, Carla [1 ]
Buss, Jackson [1 ,2 ]
Plumer, Trevor M. [1 ]
Xiao, Jie [1 ]
机构
[1] Johns Hopkins Univ, Sch Med, Dept Biophys & Biophys Chem, Baltimore, MD 21205 USA
[2] Harvard Univ, Sch Med, Dept Microbiol & Immunobiol, Boston, MA 02115 USA
基金
美国国家科学基金会; 美国国家卫生研究院;
关键词
FtsZ; superresolution; force generation; cytokinesis; cell wall synthesis; ESCHERICHIA-COLI CHROMOSOME; CELL-DIVISION GENE; Z-RING; FTSZ-RING; PEPTIDOGLYCAN SYNTHESIS; IN-VIVO; ASSEMBLY DYNAMICS; HIGH-THROUGHPUT; PROTEIN FTSZ; GROWTH-RATE;
D O I
10.1073/pnas.1514296113
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Bacterial cytokinesis is accomplished by the essential 'divisome' machinery. The most widely conserved divisome component, FtsZ, is a tubulin homolog that polymerizes into the 'FtsZ-ring' ('Z-ring'). Previous in vitro studies suggest that Z-ring contraction serves as a major constrictive force generator to limit the progression of cytokinesis. Here, we applied quantitative superresolution imaging to examine whether and how Z-ring contraction limits the rate of septum closure during cytokinesis in Escherichia coli cells. Surprisingly, septum closure rate was robust to substantial changes in all Z-ring properties proposed to be coupled to force generation: FtsZ's GTPase activity, Z-ring density, and the timing of Z-ring assembly and disassembly. Instead, the rate was limited by the activity of an essential cell wall synthesis enzyme and further modulated by a physical divisome-chromosome coupling. These results challenge a Z-ring-centric view of bacterial cytokinesis and identify cell wall synthesis and chromosome segregation as limiting processes of cytokinesis.
引用
收藏
页码:E1044 / E1053
页数:10
相关论文
共 120 条
[1]   Maturation of the Escherichia coli divisome occurs in two steps [J].
Aarsman, MEG ;
Piette, A ;
Fraipont, C ;
Vinkenvleugel, TMF ;
Nguyen-Distèche, M ;
den Blaauwen, T .
MOLECULAR MICROBIOLOGY, 2005, 55 (06) :1631-1645
[2]   Bacterial cell division: assembly, maintenance and disassembly of the Z ring [J].
Adams, David W. ;
Errington, Jeff .
NATURE REVIEWS MICROBIOLOGY, 2009, 7 (09) :642-653
[3]   FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli [J].
Addinall, SG ;
Lutkenhaus, J .
MOLECULAR MICROBIOLOGY, 1996, 22 (02) :231-237
[4]   Force generation by a dynamic Z-ring in Escherichia coli cell division [J].
Allard, Jun F. ;
Cytrynbaum, Eric N. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2009, 106 (01) :145-150
[5]   Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins [J].
Anderson, DE ;
Gueiros-Filho, FJ ;
Erickson, HP .
JOURNAL OF BACTERIOLOGY, 2004, 186 (17) :5775-5781
[6]   Evidence for Divisome Localization Mechanisms Independent of the Min System and SlmA in Escherichia coli [J].
Bailey, Matthew W. ;
Bisicchia, Paola ;
Warren, Boyd T. ;
Sherratt, David J. ;
Maennik, Jaan .
PLOS GENETICS, 2014, 10 (08)
[7]   Cooperativity of peptidoglycan synthases active in bacterial cell elongation [J].
Banzhaf, Manuel ;
van Saparoea, Bart van den Berg ;
Terrak, Mohammed ;
Fraipont, Claudine ;
Egan, Alexander ;
Philippe, Jules ;
Zapun, Andre ;
Breukink, Eefjan ;
Martine Nguyen-Disteche ;
den Blaauwen, Tanneke ;
Vollmer, Waldemar .
MOLECULAR MICROBIOLOGY, 2012, 85 (01) :179-194
[8]   THE BALANCE BETWEEN DIFFERENT PEPTIDOGLYCAN PRECURSORS DETERMINES WHETHER ESCHERICHIA-COLI-CELLS WILL ELONGATE OR DIVIDE [J].
BEGG, KJ ;
TAKASUGA, A ;
EDWARDS, DH ;
DEWAR, SJ ;
SPRATT, BG ;
ADACHI, H ;
OHTA, T ;
MATSUZAWA, H ;
DONACHIE, WD .
JOURNAL OF BACTERIOLOGY, 1990, 172 (12) :6697-6703
[9]   INTERACTION BETWEEN MEMBRANE-PROTEINS PBP3 AND RODA IS REQUIRED FOR NORMAL-CELL SHAPE AND DIVISION IN ESCHERICHIA-COLI [J].
BEGG, KJ ;
SPRATT, BG ;
DONACHIE, WD .
JOURNAL OF BACTERIOLOGY, 1986, 167 (03) :1004-1008
[10]   Imaging intracellular fluorescent proteins at nanometer resolution [J].
Betzig, Eric ;
Patterson, George H. ;
Sougrat, Rachid ;
Lindwasser, O. Wolf ;
Olenych, Scott ;
Bonifacino, Juan S. ;
Davidson, Michael W. ;
Lippincott-Schwartz, Jennifer ;
Hess, Harald F. .
SCIENCE, 2006, 313 (5793) :1642-1645