Abstract
Cell division is a key event in the bacterial life cycle. It involves constriction at the midcell, so that one cell can give rise to two daughter cells. This constriction is mediated by a ring composed of fibrous multimers of the protein FtsZ. However, a host of additional factors is involved in the formation and dynamics of this “Z-ring” and this complicated apparatus is collectively known as the “divisome”. We review the literature, with an emphasis on mathematical modelling, and show how such theoretical efforts have helped experimentalists to make sense of the at times bewildering data, and plan further experiments.
References
1.
Den Blaauwen T.
,
De Pedro M.A.
,
Nguyen-Distèche M.
, and
Ayala J.A.
(2008 ) FEMS Microbiol. Rev. , 32 , 321 –344 .
2.
Typas A.
,
Banzhaf M.
,
Gross C.A.
, and
Vollmer W.
(2011 ) Nat. Rev. Microbiol. , 10 , 123 –136 .
3.
Den Blaauwen T.
(2013 ) Curr. Opin. Microbiol. , 16 , 738 –744 .
4.
Egan A.J.F.
, and
Vollmer W.
(2013 ) Ann. N.Y. Acad. Sci. , 1277 , 8 –28 .
5.
Galli E.
, and
Gerdes K.
(2012 ) J. Bacteriol. , 194 , 292 –302 .
6.
Durand-Heredia J.M.
,
Yu H.H.
,
De Carlo S.
,
Lesser C.F.
, and
Janakiraman A.
(2011 ) J. Bacteriol. , 193 , 1405 –1413 .
7.
Durand-Heredia J.
,
Rivkin E.
,
Fan G.
,
Morales J.
, and
Janakiraman A.
(2012 ) J. Bacteriol. , 194 , 3189 –3198 .
8.
Pichoff S.
, and
Lutkenhaus J.
(2002 ) EMBO J. , 21 , 685 –693 .
9.
Van De Putte P.
,
Van Dillewijn J.
, and
Roersch A.
(1964 ) Mutat. Res. , 106 , 121 –128 .
10.
Hirota Y.
(1968 ) Cold Spring Habor Symp. Quant. Biol. , 33 , 677 –693 .
11.
Goehring N.W.
, and
Beckwith J.
(2005 ) Curr. Biol. , 15 , R514 –R526 .
12.
Allen J.S.
,
Filip C.C.
,
Gustafson R.A.
,
Allen R.G.
, and
Walker J.R.
(1974 ) J. Bacteriol. , 117 , 978 –986 .
13.
Addinall S.G.
,
Erfei B.
, and
Lutkenhaus J.
(1996 ) J. Bacteriol. , 178 , 3877 –3884 .
14.
Addinall S.G.
,
Cao C.
, and
Lutkenhaus J.
(1997 ) J. Bacteriol. , 179 , 4277 –4284 .
15.
Bi E.F.
, and
Lutkenhaus J.
(1991 ) Nature , 354 , 161 –164 .
16.
Stricker J.
,
Maddox P.
,
Salmon E.D.
, and
Erickson H.P.
(2002 ) Proc. Natl. Acad. Sci. USA , 99 , 3171 –3175 .
17.
Anderson D.E.
,
Gueiros-Filho F.J.
, and
Erickson H.P.
(2004 ) J. Bacteriol. , 186 , 5775 –5781 .
18.
Chen Y.
, and
Erickson H.P.
(2005 ) J. Biol. Chem. , 280 , 22549 –22554 .
19.
Schmidt K.L.
,
Peterson N.D.
,
Kustusch R.J.
,
Wissel M.C.
,
Graham B.
,
Phillips G.J.
, and
Weiss G.S.
(2004 ) J. Bacteriol. , 186 , 785 –793 .
20.
Corbin B.D.
,
Wang Y.
,
Beuria T.K.
, and
Margolin W.
(2007 ) J. Bacteriol. , 189 , 3026 –3935 .
21.
Wang L.
, and
Lutkenhaus J.
(1998 ) Mol. Microbiol. , 29 , 731 –740 .
22.
Chen J.
, and
Beckwith J.
(2001 ) Mol. Microbiol. , 42 , 395 –413 .
23.
Chen J.
,
Weiss D.
,
Ghigo J.
, and
Beckwith J.
(1999 ) J. Bacteriol. , 181 , 521 –530 .
24.
Ghigo J.
,
Weiss D.
,
Chen J.
,
Yarrow J.
, and
Beckwith J.
(1999 ) Mol. Microbiol. , 31 , 725 –737 .
25.
Mercer K.
, and
Weiss D.
(2002 ) J. Bacteriol. , 184 , 904 –912 .
26.
Weiss D.
,
Chen J.
,
Ghigo J.
,
Boyd D.
, and
Beckwith J.
(1999 ) J. Bacteriol. , 181 , 508 –520 .
27.
Aarsman M.E.G.
,
Piette A.
,
Fraipont C.
,
Vinkenvleugel T.M.F.
,
Nguyen-Distèche M.
, and
Den Blaauwen T.
(2005 ) Mol. Microbiol. , 55 , 1631 –1645 .
28.
Goehring N.W.
,
Gueiros-Filho F.
, and
Beckwith J.
(2005 ) Genes Dev. , 19 , 127 –137 .
29.
Fraipont C.
,
Alexeeva S.
,
Wolf B.
,
van der Ploeg R.
,
Schloesser M.
,
Den Blaauwen T.
, and
Nguyen-Distèche M.
(2011 ) Microbiology. , 157 , 251 –259 .
30.
Buddelmeijer N.
, and
Beckwith J.
(2004 ) Mol. Microbiol. , 52 , 1315 –1327 .
31.
Geissler B.
, and
Margolin W.
(2005 ) Mol. Microbiol. , 58 , 596 –612 .
32.
Cordell S.C.
,
Robinson E.J.H.
, and
Lowe J.
(2003 ) Proc. Natl. Acad. Sci. USA , 100 , 7889 –7894 .
33.
Erickson H.P.
,
Anderson D.E.
, and
Osawa M.
(2010 ) Microbiol. Mol. Biol. Rev. , 74 , 504 –528 .
34.
RayChaudhuri D.
, and
Park J.T.
(1992 ) Nature , 359 , 251 –254 .
35.
De Boer P.
,
Crossley R.
, and
Rothfield L.
(1992 ) Nature , 359 , 254 –256 .
36.
Löwe J.
, and
Amos L.A.
(1998 ) Nature , 391 , 203 –206 .
37.
Nogales E.
,
Wolf S.G.
, and
Downing K.H.
(1998 ) Nature , 391 , 199 –203 .
38.
Scheffers D.J.
,
De Wit J.G.
,
Den Blaauwen T.
, and
Driessen A.J.M.
(2002 ) Biochemistry , 41 , 521 –529 .
39.
Scheffers D.J.
,
De Wit J.G.
,
Den Blaauwen T.
, and
Driessen A.J.M.
(2001 ) FEBS Lett. , 494 , 34 –37 .
40.
Mukherjee A.
, and
Lutkenhaus J.
(1998 ) EMBO J. , 17 , 462 –469 .
41.
Erickson H.P.
,
Taylor D.W.
,
Taylor K.A.
, and
Bramhill D.
(1996 ) Proc. Natl. Acad. Sci. USA , 93 , 519 –523 .
42.
Yu X.
, and
Margolin W.
(1997 ) EMBO J. , 16 , 5455 –5463 .
43.
Bramhill D.
, and
Thompson C.M.
(1994 ) Proc. Natl. Acad. Sci. USA , 91 , 5813 –5817 .
44.
Chen Y.
,
Bjornson K.
,
Redick S.
,
Erickson H.
(2005 ) Biophys. J. , 88 , 505 –514 .
45.
González J.M.
,
Jiménez M.
,
Vélez M.
,
Mingorance J.
,
Andreu J.M.
,
Vicente M.
, and
Rivas G.
(2003 ) J. Biol. Chem. , 278 , 37664 –37671 .
46.
Popp D.
,
Iwasa M.
,
Narita A.
,
Erickson H.P.
, and
Maéda Y.
(2009 ) Biopolymers , 91 , 340 –350 .
47.
Huecas S.
,
Llorca O.
,
Boskovic J.
,
Martín-Benito J.
,
Valpuesta J.M.
, and
Andreu J.M.
(2008 ) Biophys. J. , 94 , 1796 –1806 .
48.
Romberg L.
,
Simon M.
, and
Erickson H.P.
(2001 ) J. Biol. Chem. , 276 , 11743 –11753 .
49.
Caplan M.R.
, and
Erickson H.P.
(2003 ) J. Biol. Chem. , 278 , 13784 –13788 .
50.
Rueda S.
,
Vicente M.
, and
Mingorance J.
(2003 ) J. Bacteriol. , 185 , 3344 –3351 .
51.
Pla J.
,
Sánchez M.
,
Palacios P.
,
Vicente M.
, and
Aldea M.
(1991 ) Mol. Microbiol. , 5 , 1681 –1686 .
52.
Lu C.
,
Stricker J.
, and
Erickson H.P.
(1998 ) Cell Motil. Cytoskeleton , 40 , 71 –86 .
53.
González J.M.
,
Vélez M.
,
Jiménez M.
,
Alfonso C.
,
Schuck P.
,
Mingorance J.
,
Vicente M.
,
Minton A.P.
, and
Rivas G.
(2005 ) Proc. Natl. Acad. Sci. USA , 102 , 1895 –1900 .
54.
Miraldi E.R.
,
Thomas P.J.
, and
Romberg L.
(2008 ) Biophys. J. , 95 , 2470 –2486 .
55.
Addinall S.
, and
Lutkenhaus J.
(1996 ) Mol. Microbiol. , 22 , 231 –237 .
56.
Fu G.
,
Huang T.
,
Buss J.
,
Coltharp C.
,
Hensel Z.
, and
Xiao J.
(2010 ) PLoS One , 5 , 1 –16 .
57.
Sun Q.
, and
Margolin W.
(1998 ) J. Bacteriol. , 180 , 2050 –2056 .
58.
Ma X.
,
Ehrhardt D.W.
, and
Margolin W.
(1996 ) Proc. Natl. Acad. Sci. USA , 93 , 12998 –13003 .
59.
Thanedar S.
, and
Margolin W.
(2004 ) Curr. Biol. , 14 , 1167 –1173 .
60.
Peters P.C.
,
Migocki M.D.
,
Thoni C.
, and
Harry E.J.
(2007 ) Mol. Microbiol. , 64 , 487 –499 .
61.
Jennings P.C.
,
Cox G.C.
,
Monahan L.G.
, and
Harry E.J.
(2011 ) Micron. , 42 , 336 –341 .
62.
Niu L.
, and
Yu J.
(2008 ) Biophys. J. , 95 , 2009 –2016 .
63.
Margolin W.
(2012 ) J. Bacteriol. , 194 , 6369 –6371 .
64.
Swulius M.
, and
Jensen G.
(2012 ) J. Bacteriol. , 194 , 6382 –6386 .
65.
Rowlett V.
, and
Margolin W.
(2014 ) Biophys. J. , 107 , L17 –L20 .
66.
Strauss M.P.
,
Liew A.T.F.
,
Turnbull L.
,
Whitchurch C.B.
,
Monahan L.G.
, and
Harry E.J.
(2012 ) PLoS Biol. , 10 e1001389 .
67.
Holden S.J.
,
Pengo T.
,
Meibom K.L.
,
Fernandez Fernandez C.
, and
Collier J.
,
Manley S.
(2014 ) Proc. Natl. Acad. Sci. USA , 111 , 4566 –4571 .
68.
Li Z.
,
Trimble M.J.
,
Brun Y.V.
, and
Jensen G.J.
(2007 ) EMBO J. , 26 , 4694 –4708 .
69.
Osawa M.
,
Anderson D.E.
, and
Erickson H.P.
(2008 ) Science , 320 , 792 –794 .
70.
Osawa M.
,
Anderson D.E.
, and
Erickson H.P.
(2009 ) EMBO J. , 28 , 3476 –3484 .
71.
Osawa M.
, and
Erickson H.P.
(2011 ) Mol. Microbiol. , 81 , 571 –579 .
72.
Milam S.L.
,
Osawa M.
, and
Erickson H.P.
(2012 ) Biophys. J. , 103 , 59 –68 .
73.
Maupin P.
, and
Pollard T.
(1986 ) J. Ultrastruct. Mol. Struct. Res. , 94 , 92 –103 .
74.
Lan G.
,
Wolgemuth C.W.
, and
Sun S.X.
(2007 ) Proc. Natl. Acad. Sci. USA , 104 , 16110 –16115 .
75.
Erickson H.P.
(2009 ) Proc. Natl. Acad. Sci. USA , 106 , 9238 –9243 .
76.
Lu C.
,
Reedy M.
, and
Erickson H.P.
(2000 ) J. Bacteriol. , 182 , 164 –170 .
77.
Mingorance J.
,
Tadros M.
,
Vicente M.
,
González J.M.
,
Rivas G.
, and
Vélez M.
(2005 ) J. Biol. Chem. , 280 , 20909 –20914 .
78.
Li Y.
,
Hsin J.
,
Zhao L.
,
Cheng Y.
,
Shang W.
,
Huang K.C.
,
Wang H.W.
, and
Ye S.
(2013 ) Science , 341 , 392 –395 .
79.
Hsin J.
,
Gopinathan A.
, and
Huang K.C.
(2012 ) Proc. Natl. Acad. Sci. USA , 109 , 9432 –9437 .
80.
Bailey M.
,
Bisicchia P.
,
Warren B.
,
Sherratt D.
, and
Mannik J.
(2014 ) PLOS Genet. , 10 , e1004504 .
81.
Tsang M.
, and
Bernhardt T.G.
(2015 ) Curr. Opin. Microbiol. , 24 , 60 –65 .
82.
Janion C.
(2008 ) Int. J. Biol. Sci. , 4 , 338 –344 .
83.
Huisman O.
,
D'Ari R.
, and
Gottesman S.
(1984 ) Proc. Natl. Acad. Sci. USA , 81 , 4490 –4494 .
84.
Dajkovic A.
,
Mukherjee A.
,
Lutkenhaus J.
(2008 ) J. Bacteriol. , 190 , 2513 –2526 .
85.
Chen Y.
,
Milam S.L.
, and
Erickson H.P.
(2012 ) Biochemistry , 51 , 3100 –3109 .
86.
Mukherjee A.
,
Cao C.
, and
Lutkenhaus J.
(1998 ) Proc. Natl. Acad. Sci. USA , 95 , 2885 –2890 .
87.
Mizusawa S.
, and
Gottesman S.
(1983 ) Proc. Natl. Acad. Sci. USA , 80 , 358 –362 .
88.
De Boer P.A.
,
Crossley R.E.
, and
Rothfield L.I.
(1989 ) coli. Cell , 56 , 641 –649 .
89.
De Boer P.A.
,
Crossley R.E.
, and
Rothfield L.I.
(1990 ) Proc. Natl. Acad. Sci. USA , 87 , 1129 –1133 .
90.
Bi E.
, and
Lutkenhaus J.
(1990 ) J. Bacteriol. , 172 , 2765 –2768 .
91.
Lutkenhaus J.
(2007 ) Ann. Rev. Biochem. , 76 , 539 –562 .
92.
Raskin D.M.
, and
de Boer P.A.
(1999 ) Proc. Natl. Acad. Sci. USA , 96 , 4971 –4976 .
93.
Hale C.
,
Meinhardt H.
, and
de Boer P.
(2001 ) EMBO J. , 20 , 1563 –1572 .
94.
Hu Z.
, and
Lutkenhaus J.
(1999 ) Mol. Microbiol. , 34 , 82 –90 .
95.
Hu Z.
,
Mukherjee A.
,
Pichoff S.
, and
Lutkenhaus J.
(1999 ) Proc. Natl. Acad. Sci. USA , 96 , 14819 –14824 .
96.
De Boer P.
,
Crossley R.
,
Hand A.
, and
Rothfield L.
(1991 ) EMBO J. , 10 , 4371 –4380 .
97.
Hu Z.
,
Saez C.
, and
Lutkenhaus J.
(2003 ) J. Bacteriol. , 185 , 196 –203 .
98.
Szeto T.H.
,
Rowland S.L.
,
Rothfield L.I.
, and
King G.F.
(2002 ) Proc. Natl. Acad. Sci. USA , 99 , 15693 –15698 .
99.
Hu Z.
, and
Lutkenhaus J.
(2003 ) Mol. Microbiol. , 47 , 345 –355 .
100.
Hu Z.
, and
Lutkenhaus J.
(2001 ) Mol. Cell. , 7 , 1337 –1343 .
101.
Lackner L.L.
,
Raskin D.M.
,
De Boer P.A.J.
(2003 ) J. Bacteriol. , 185 , 735 –749 .
102.
Huang K.C.
,
Meir Y.
,
Wingreen N.S.
(2003 ) Proc. Natl. Acad. Sci. USA , 100 , 12724 –12728 .
103.
Wu L.J.
, and
Errington J.
(2012 ) Nat. Rev. Microbiol. , 10 , 8 –12 .
104.
Wu L.J.
, and
Errington J.
(2004 ) Cell , 117 , 915 –925 .
105.
Bernhardt T.G.
, and
de Boer P.
(2005 ) Mol. Cell. , 18 , 555 –564 .
106.
Wu L.J.
,
Ishikawa S.
,
Kawai Y.
,
Oshima T.
,
Ogasawara N.
, and
Errington J.
(2009 ) EMBO J. , 28 , 1940 –1952 .
107.
Tonthat N.K.
,
Arold S.T.
,
Pickering B.F.
,
Van Dyke M.W.
,
Liang S.
,
Lu Y.
,
Beuria T.K.
,
Margolin W.
, and
Schumacher M.A.
(2011 ) EMBO J. , 30 , 154 –164 .
108.
Tonthat N.K.
,
Milam S.L.
,
Chinnam N.
,
Whitfill T.
,
Margolin W.
, and
Schumacher M.A.
(2013 ) Proc. Natl. Acad. Sci. USA , 110 , 10586 –10591 .
109.
Cho H.
,
McManus H.R.
,
Dove S.L.
, and
Bernhardt T.G.
(2011 ) Proc. Natl. Acad. Sci. USA , 108 , 3773 –3778 .
110.
Du S.
, and
Lutkenhaus J.
(2014 ) PLoS Genet. , 10 , e1004460 .
111.
Mercier R.
,
Petit M.
,
Schbath S.
,
Robin S.
,
El Karoui M.
,
Boccard F.
, and
Espéli O.
(2008 ) Cell , 135 , 475 –485 .
112.
Espéli O.
,
Borne R.
,
Dupaigne P.
,
Thiel A.
,
Gigant E.
,
Mercier R.
, and
Boccard F.
(2012 ) EMBO J. , 31 , 3198 –3211 .
113.
Hale C.A.
, and
De Boer P.A.J.
(1997 ) Cell , 88 , 175 –185 .
114.
RayChaudhuri D.
(1999 ) EMBO J. , 18 , 2372 –2383 .
115.
Liu Z.
,
Mukherjee A.
, and
Lutkenhaus J.
(1999 ) Mol. Microbiol. , 31 , 1853 –1861 .
116.
Moy F.J.
,
Glasfeld E.
,
Mosyak L.
, and
Powers R.
(2000 ) Biochemistry , 39 , 9146 –9156 .
117.
Mosyak L.
,
Zhang Y.
,
Glasfeld E.
,
Haney S.
,
Stahl M.
,
Seehra J.
, and
Somers W.S.
(2000 ) EMBO J. , 19 , 3179 –3191 .
118.
Pichoff S.
, and
Lutkenhaus J.
(2005 ) Mol. Microbiol. , 55 , 1722 –1734 .
119.
Addinall S.G.
, and
Lutkenhaus J.
(1996 ) J. Bacteriol. , 178 , 7167 –7172 .
120.
Karimova G.
,
Dautin N.
, and
Ladant D.
(2005 ) J. Bacteriol. , 187 , 2233 –2243 .
121.
Bork P.
,
Sander C.
, and
Valencia A.
(1992 ) Proc. Natl. Acad. Sci. USA , 89 , 7290 –7294 .
122.
Lara B.
,
Rico A.I.
,
Petruzzelli S.
,
Santona A.
,
Dumas J.
,
Biton J.
,
Vicente M.
,
Mingorance J.
, and
Massidda O.
(2005 ) Mol. Microbiol. , 55 , 699 –711 .
123.
Feucht A.
,
Lucet I.
,
Yudkin M.D.
, and
Errington J.
(2001 ) Mol. Microbiol. , 40 , 115 –125 .
124.
Van den Ent F.
,
Amos L.A.
, and
Löwe J.
(2001 ) Nature , 413 , 39 –44 .
125.
Loose M.
, and
Mitchison T.J.
(2014 ) Nature Cell Biol. , 16 , 38 –46 .
126.
van den Berg H.A.
(2011 ) Mathematical models of biological systems. Oxford University Press .
127.
Doucet P.
, and
Sloep P.
(1992 ) Mathematical modeling in the life sciences , Wiley , New York .
128.
Oosawa F.
, and
Kasai M.
(1962 ) J. Mol. Biol. , 4 , 10 –21 .
129.
Allard J.F.
, and
Cytrynbaum E.N.
(2009 ) Proc. Natl. Acad. Sci. USA , 106 , 145 –150 .
130.
Lan G.
,
Daniels B.R.
,
Dobrowsky T.M.
,
Wirtz D.
, and
Sun S.X.
(2009 ) Proc. Natl. Acad. Sci. USA , 106 , 121 –126 .
131.
Surovtsev I.V.
,
Morgan J.J.
, and
Lindahl P.A.
(2008 ) PLoS Comput. Biol. , 4 , e1000102 .
132.
Zhang Z.
,
Morgan J.J.
, and
Lindahl P.A.
(2014 ) J. Math. Biol. , 68 , 911 –930 .
133.
Loose M.
,
Fischer-Friedrich E.
,
Ries J.
,
Kruse K.
, and
Schwille P.
(2008 ) Science , 320 , 789 –792 .
134.
Meinhardt H.
, and
de Boer P.A.
(2001 ) Proc. Natl. Acad. Sci. USA , 98 , 14202 –14207 .
135.
Dow C.E.
,
Rodger A.
,
Roper D.I.
, and
van den Berg H.A.
(2013 ) Integr. Biol. , 5 , 778 –795 .
136.
Ma X.L.
, and
Margolin W.
(1999 ) J. Bacteriol. , 181 , 7531 –7544 .
137.
Haney S.A.
,
Glasfeld E.
,
Hale C.
,
Keeney D.
,
He Z.
, and
De Boer P.
(2001 ) J. Biol. Chem. , 276 , 11980 –11987 .
138.
Hale C.A.
, and
De Boer P.A.J.
(1999 ) J. Bacteriol. , 181 , 167 –176 .
139.
Läppchen T.
(2007 ) Synthesis of GTP analogues and evaluation of their effect on the antibiotic target FtsZ and its eukaryotic homologue tubulin , University of Amsterdam .
140.
Marcelo F.
,
Huecas S.
,
Ruiz-ávila L.B.
,
Cañada F.J.
,
Perona A.
,
Poveda A.
,
Martín-Santamaría S.
,
Morreale A.
,
Jiménez-Barbero J.
, and
Andreu J.M.
(2013 ) J. Am. Chem. Soc. , 135 , 16418 –16428 .
141.
Duggirala S.
,
Nankar R.P.
,
Rajendran S.
, and
Doble M.
(2014 ) Appl. Biochem. Biotechnol. , 174 , 283 –296 .
142.
Lu C.
,
Stricker J.
, and
Erickson H.P.
(2001 ) BMC Microbiol. , 1 , 7 .
143.
Phoenix P.
, and
Drapeau G.
(1988 ) J. Bacteriol. , 170 , 4338 –4342 .
144.
Stricker J.
, and
Erickson H.P.
(2003 ) J. Bacteriol. , 185 , 4796 –4805 .
145.
RayChaudhuri D.
, and
Park J.T.
(1994 ) J. Biol. Chem. , 269 , 22941 –22944 .
146.
Dow C.E.
,
van den Berg H.A.
,
Roper D.I.
, and
Rodger A.
(2015 ) Biochemistry , 54 , 3803 –3813 .
147.
Oliva M.A.
,
Trambaiolo D.
, and
Löwe J.
(2007 ) J. Mol. Biol. , 373 , 1229 –1242 .