Do the divisome and elongasome share a common evolutionary past?

Current Opinion in Microbiology

Volumn 16, Issue 6, 2013, Pages 745-751

  Szwedziak, Piotr ^a   Löwe, Jan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CARRIER PROTEIN; DISACCHARIDE; DIVISOME; ELONGASOME; ENVC PROTEIN; FTSA PROTEIN; FTSK PROTEIN; FTSN PROTEIN; FTSQ PROTEIN; FTSW PROTEIN; GAMMA GLUTAMYLTRANSFERASE; GLYCAN; GLYCOSYLTRANSFERASE; LIPID; LIPID II; MEMBRANE PROTEIN; MEMBRANE PROTEIN MRAY; MEMBRANE PROTEIN MURF; MEMBRANE PROTEIN MURG; MREB PROTEIN; MREC PROTEIN; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 2; PEPTIDOGLYCAN; RODA PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; BACILLUS SUBTILIS; CARBOXY TERMINAL SEQUENCE; CELL DIVISION; CELL ELONGATION; CELL MEMBRANE; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME ACTIVITY; FEEDBACK SYSTEM; HYDROLYSIS; LIPID TRANSPORT; LIPOGENESIS; MOLECULAR EVOLUTION; NONHUMAN; POLYMERIZATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS);

BACTERIAL PROTEINS; CELL DIVISION; CELL WALL; GRAM-NEGATIVE BACTERIA; METABOLIC NETWORKS AND PATHWAYS; PEPTIDOGLYCAN;

EID: 84888203647     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2013.09.003     Document Type: Review

References (66)

1. Typas A., Banzhaf M., Gross C.A., Vollmer W. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat Rev Microbiol 2011, 10:123-136.
2. Adams D.W., Errington J. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 2009, 7642-7653.
3. Lutkenhaus J., Pichoff S., Du S. Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton (Hoboken) 2012, 69:778-790.
4. den Blaauwen T., de Pedro M.A., Nguyen-Disteche M., Ayala J.A. Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev 2008, 32:321-344.
5. Bouhss A., Trunkfield A.E., Bugg T.D., Mengin-Lecreulx D. The biosynthesis of peptidoglycan lipid-linked intermediates. FEMS Microbiol Rev 2008, 32:208-233.
6. Mohammadi T., Karczmarek A., Crouvoisier M., Bouhss A., Mengin-Lecreuix D., den Blaauwen T. The essential peptidoglycan glycosyltransferase MurG forms a complex with proteins involved in lateral envelope growth as well as with proteins involved in cell division in Escherichia coli. Mol Microbiol 2007, 65:1106-1121.
7. Favini-Stabile S., Contreras-Martel C., Thielens N., Dessen A. MreB and MurG as scaffolds for the cytoplasmic steps of peptidoglycan biosynthesis. Environ Microbiol 2013.
8. White C.L., Kitich A., Gober J.W. Positioning cell wall synthetic complexes by the bacterial morphogenetic proteins MreB and MreD. Mol Microbiol 2010, 76:616-633.
9. Ikeda M., Sato T., Wachi M., Jung H.K., Ishino F., Kobayashi Y., Matsuhashi M. Structural similarity among Escherichia coli FtsW and RodA proteins and Bacillus subtilis SpoVE protein, which function in cell division, cell elongation, and spore formation, respectively. J Bacteriol 1989, 171:6375-6378.
10. Gerard P., Vernet T., Zapun A. Membrane topology of the Streptococcus pneumoniae FtsW division protein. J Bacteriol 2002, 184:1925-1931.
11. Mohammadi T., van Dam V., Sijbrandi R., Vernet T., Zapun A., Bouhss A., Diepeveen-de Bruin M., Nguyen-Disteche M., de Kruijff B., Breukink E. Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane. EMBO J 2011, 301:425-1432.
12. Shiomi D., Toyoda A., Aizu T., Ejima F., Fujiyama A., Shini T., Kohara Y., Niki H. Mutations in cell elongation genes mreB, mrdA and mrdB suppress the shape defect of RodZ-deficient cells. Mol Microbiol 2013, 87:1029-1044.
13. Spratt B.G. Distinct penicillin binding proteins involved in the division, elongation, and shape of Escherichia coli K12. Proc Natl Acad Sci USA 1975, 72:2999-3003.
14. Potluri L., Karczmarek A., Verheul J., Piette A., Wilkin J.M., Werth N., Banzhaf M., Vollmer W., Young K.D., Nguyen-Disteche M., den Blaauwen T. Septal and lateral wall localization of PBP5, the major d,d-carboxypeptidase of Escherichia coli, requires substrate recognition and membrane attachment. Mol Microbiol 2010, 77:300-323.
15. van der Ploeg R., Verheul J., Visher N.O.E., Alexeeva S., Hoogendoorn E., Postma M., Banzhaf M., Vollmer W., den Blaauwen T. Colocalization and interaction between elongasome and divisome during a preparative cell division in Escherichia coli. Mol Microbiol 2013, 87:1074-1087.
16. Fraipont C., Alexeeva S., Wolf B., van der Ploeg R., Schloesser M., den Blaauwen T., Nguyen-Disteche M. The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli. Microbiology 2011, 157:251-259.
17. Bertsche U., Kast T., Wolf B., Fraipont C., Aarsman M.E., Kannenberg K., von Rechenberg M., Nguyen-Disteche M., den Blaauwen T., Holtje J.V., Vollmer W. Interaction between two murein (peptidoglycan) synthases, PBP3 and PBP1B, in Escherichia coli. Mol Microbiol 2006, 61:675-690.
18. Sung M.T., Lai Y.T., Huang C.Y., Chou L.Y., Shih H.W., Cheng W.C., Wong C.H., Ma C. Crystal structure of the membrane-bound bifunctional transglycosylase PBP1b from Escherichia coli. Proc Natl Acad Sci USA 2009, 106:8824-8829.
19. Lovering A.L., de Castro L.H., Lim D., Strynadka N.C. Structural insight into the transglycosylation step of bacterial cell-wall biosynthesis. Science 2007, 315:1402-1405.
20. van den Ent F., Amos L.A., Löwe J. Prokaryotic origin of the actin cytoskeleton. Nature 2001, 413:39-44.
21. Salje J., van den Ent F., de Boer P.A.J., Löwe J. Direct membrane binding by bacterial actin MreB. Mol Cell 2011, 43:478-487.
22. van den Ent F., Löwe: J. Crystal structure of the cell division protein FtsA from Thermotoga maritima. EMBO J 2000, 19:5300-5307.
23. Pichoff S., Lutkenhaus: J. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 2005, 55:1722-1734.
24. Krupka M., Rivas G., Rico A.I., Vicente M. Key role of two terminal domains in the bidirectional polymerization of FtsA protein. J Biol Chem 2012, 287:7756-7765.
25. Lara B., Rico A.I., Petruzzelli S., Santona A., Dumas J., Biton J., Vicente M., Mingorance J., Massidda O. Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol Microbiol 2005, 55:699-711.
26. Szwedziak P., Wang Q., Freund S.M., Löwe J. FtsA forms actin-like filaments. EMBO J 2012, 31:2249-2260.
27. 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 2003, 100:4197-4202.
28. Vicente M., Rico: A.I. The order of the ring: assembly of Escherichia coli cell division components. Mol Microbiol 2006, 61:5-8.
29. 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 2012, 194:1989-2000.
30. Karuppiah V., Derrick: J.P. Structure of the PilM-PilN inner membrane type IV pilus biogenesis complex from Thermus thermophilus. J Biol Chem 2011, 286:24434-24442.
31. Kruse T., Bork-Jensen J., Gerdes K. The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 2005, 55:78-89.
32. Dominguez-Escobar J., Chastanet A., Crevenna A.H., Fromion V., Wedlich-Soldner R., Carballido-Lopez R. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 2011, 333:225-228.
33. Garner E.C., Bernard R., Wang W., Zhuang X., Rudner D.Z., Mitchison T. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 2011, 333:222-225.
34. van Teeffelen S., Wang S., Furchtgott L., Huang K.C., Wingreen N.S., Shaevitz J.W., Gitai Z. The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci USA 2011, 108:15822-15827.
35. Osawa M., Anderson D.E., Erickson H.P. Reconstitution of contractile FtsZ rings in liposomes. Science 2008, 320:792-794.
36. Osawa M., Erickson: H.P. Liposome division by a simple bacterial division machinery. Proc Natl Acad Sci USA 2013, 110:11000-11004.
37. Buddelmeijer N., Beckwith: J. A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol Microbiol 2004, 52:1315-1327.
38. 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 2007, 63:1008-1025.
39. Schmidt K.L., Peterson N.D., Kustusch R.J., Wissel M.C., Graham B., Phillips G.J., Weiss D.S. A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J Bacteriol 2004, 186:785-793.
40. Yang D.C., Peters N.T., Parzych K.R., Uehara T., Markovski M., Bernhardt T.G. An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring. Proc Natl Acad Sci USA 2011, 108:E1052-E1060.
41. Bernhardt T.G., de Boer P.A.J. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol Microbiol 2003, 48:1171-1182.
42. Carballido-Lopez R., Formstone A., Li Y., Ehrlich S.D., Noirot P., Errington J. Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 2006, 11:399-409.
43. Typas A., Banzhaf M., van den Berg van Saparoea B., Verheul J., Biboy J., Nichols R.J., Zietek M., Beilharz K., Kannenberg K., von Rechenberg M., et al. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 2010, 143:1097-1109.
44. Paradis-Bleau C., Markovski M., Uehara T., Lupoli T.J., Walker S., Kahne D.E., Bernhardt T.G. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 2010, 143:1110-1120.
45. Turner R.D., Hurd A.F., Cadby A., Hobbs J.K., Foster S.J. Cell wall elongation mode in Gram-negative bacteria is determined by peptidoglycan architecture. Nat Commun 2013, 10.1038/ncomms2503.
46. Aussel L., Barre F.X., Aroyo M., Stasiak A., Stasiak A.Z., Sherratt D. FtsK is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 2002, 108:195-205.
47. Makarova K.S., Yutin N., Bell S.D., Koonin E.V. Evolution of diverse cell division and vesicle formation systems in Archaea. Nat Rev Microbiol 2010, 8:731-741.
48. Gundogdu M.E., Kawai Y., Pavlendova N., Ogasawara N., Errington J., Scheffers D.J., Hamoen L.W. Large ring polymers align FtsZ polymers for normal septum formation. EMBO J 2011, 30:617-626.
49. Krol E., van Kessel S.P., van Bezouwen L.S., Kumar N., Boekema E.J., Scheffers D.J. Bacillus subtilis SepF binds to the C-terminus of FtsZ. PLoS ONE 2012, 7e43293.
50. Holtje J.V. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 1998, 62:181-203.
51. Aaron M., Charbon G., Lam H., Schwarz H., Vollmer W., Jacobs-Wagner C. The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol Microbiol 2007, 64:938-952.
52. Varma A., de Pedro M.A., Young K.D. FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli. J Bacteriol 2007, 189:5692-5704.
53. Vats P., Shih Y.L., Rothfield L. Assembly of the MreB-associated cytoskeletal ring of Escherichia coli. Mol Microbiol 2009, 72:170-182.
54. Fenton A.K., Gerdes: K. Direct interaction of FtsZ and MreB is required for septum synthesis and cell division in Escherichia coli. EMBO J 2013, 32:1953-1965.
55. Low H.H., Moncrieffe M.C., Löwe J. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J Mol Biol 2004, 341:839-852.
56. Matsui T., Yamane J., Mogi N., Yamaguchi H., Takemoto H., Yao M., Tanaka I. Structural reorganization of the bacterial cell-division protein FtsZ from Staphylococcus aureus. Acta Crystallogr, Sec D 2012, 68:1175-1188.
57. Mosyak L., Zhang Y., Glasfeld E., Haney S., Stahl M., Seehra J., Somers W.S. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J 2000, 19:3179-3191.
58. Massey T.H., Mercogliano C.P., Yates J., Sheratt D.J., Löwe J. Double-stranded DNA translocation: structure and mechanism of hexameric FtsK. Mol Cell 2006, 23:457-469.
59. Sivanathan V., Allen M.D., de Bekker C., Baker R., Arciszewska L.K., Freund S.M., Bycroft M., Löwe J., Sheratt D.J. The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS. Nat Struct Mol Biol 2006, 13:965-972.
60. Yang J.C., van den ent F., Neuhaus D., Brevier J., Löwe J. Solution structure and domain architecture of the divisome protein FtsN. Mol Microbiol 2004, 52:651-660.
61. Han S., Zaniewski R.P., Marr E.S., Lacey B.M., Tomaras A.P., Evdokimov A., Miller J.R., Shanmugasundaram V. Structural basis for effectiveness of siderophore-conjugated monocarbams against clinically relevant strains of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2010, 107:22002-22007.
62. Lapointe L.M., Taylor K.C., Subramaniam S., Khadria A., Rayment I., Senes A. Structural organization of FtsB, a transmembrane protein of the bacterial divisome. Biochemistry 2013, 10.1021/bi400222r.
63. van den Ent F., Vinkenvieugel T.M., Ind A., West P., Veprintsev D., Nanninga N., den Blaauwen T., Löwe J. Structural and mutational analysis of the cell division protein FtsQ. Mol Microbiol 2008, 68:110-123.
64. van den Ent F., Johnson C.M., Persons L., de Boer P.A.J., Löwe J. Bacterial actin MreB assembles in complex with cell shape protein RodZ. EMBO J 2010, 29:1081-1090.
65. van den Ent F., Leaver M., Bendezu F., Errington J., de Boer P.A.J., Löwe J. Dimeric structure of the cell shape protein MreC and its functional implications. Mol Microbiol 2006, 62:1631-1642.
66. Vijayalakshmi J., Akerley B.J., Saper M.A. Structure of YraM, a protein essential for growth of Haemophilus influenzae. Proteins 2008, 73:204-217.