Bactofilins, a ubiquitous class of cytoskeletal proteins mediating polar localization of a cell wall synthase in Caulobacter crescentus

EMBO Journal

Volumn 29, Issue 2, 2010, Pages 327-339

  Kühn, Juliane ^a,b   Briegel, Ariane ^c,d   Mörschel, Erhard ^b   Kahnt, Jörg ^a   Leser, Katja ^a,b   Wick, Stephanie ^a,b   Jensen, Grant J ^c,d   Thanbichler, Martin ^a,b  

^a MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c California Institute of Technology HHMI   (United States)

^d CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cytoskeleton; Myxococcus xanthus; Penicillinbinding protein; Peptidoglycan; Stalk

Indexed keywords

ACTIN; BACTOFILIN DERIVATIVE; CYTOSKELETON PROTEIN; MOLECULAR SCAFFOLD; PEPTIDOGLYCAN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL WALL; CAULOBACTER CRESCENTUS; CELL DIVISION; CELL MEMBRANE; CONTROLLED STUDY; CYTOSKELETON; INTERMEDIATE FILAMENT; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

BACTERIAL PROTEINS; CAULOBACTER CRESCENTUS; CELL WALL; CONSERVED SEQUENCE; CYTOSKELETAL PROTEINS; CYTOSKELETON; PENICILLIN-BINDING PROTEINS; PHYLOGENY; PROTEIN TRANSPORT;

CAULOBACTER VIBRIOIDES; EUKARYOTA; MYXOCOCCUS XANTHUS; PROKARYOTA;

EID: 75049083437     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.358     Document Type: Article

References (79)

1. Aaron M, Charbon G, Lam H, Schwarz H, Vollmer W, Jacobs-Wagner C (2007) The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol Microbiol 64: 938-952
2. Alyahya SA, Alexander R, Costa T, Henriques AO, Emonet T, Jacobs-Wagner C (2009) RodZ, a component of the bacterial core morphogenic apparatus. Proc Natl Acad Sci USA 106: 1239-1244
3. Anderson DE, Gueiros-Filho FJ, Erickson HP (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J Bacteriol 186: 5775-5781
4. Ausmees N, Kuhn JR, Jacobs-Wagner C (2003) The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115: 705-713
5. Bagchi S, Tomenius H, Belova LM, Ausmees N (2008) Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol Microbiol 70: 1037-1050
6. Ben-Yehuda S, Rudner DZ, Losick R (2003) RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299: 532-536
7. Bi EF, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164
8. Bowman GR, Comolli LR, Zhu J, Eckart M, Koenig M, Downing KH, Moerner WE, Earnest T, Shapiro L (2008) A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134: 945-955
9. Briegel A, Dias DP, Li Z, Jensen RB, Frangakis AS, Jensen GJ (2006) Multiple large filament bundles observed in Caulobacter crescen-tus by electron cryotomography. Mol Microbiol 62: 5-14
10. Burchard AC, Burchard RP, Kloetzel JA (1977) Intracellular, periodic structures in the gliding bacterium Myxococcus xanthus. J Bacteriol 132: 666-672
11. Cabeen MT, Charbon G, Vollmer W, Born P, Ausmees N, Weibel DB, Jacobs-Wagner C (2009) Bacterial cell curvature through mechanical control of cell growth. EMBO J 28: 1208-1219
12. Cabeen MT, Jacobs-Wagner C (2007) Skin and bones: the bacterial cytoskeleton, cell wall, and cell morphogenesis. J Cell Biol 179: 381-387
13. Carballido-Lopez R (2006) The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev 70: 888-909
14. Carballido-Lopez R, Errington J (2003) The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev Cell 4: 19-28
15. Carballido-Lopez R, Formstone A, Li Y, Ehrlich SD, Noirot P, Errington J (2006) Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 11: 399-409
16. Charbon G, Cabeen MT, Jacobs-Wagner C (2009) Bacterial intermediate filaments: in vivo assembly, organization, and dynamics of crescentin. Genes Dev 23: 1131-1144
17. Defeu Soufo HJ, Graumann PL (2006) Dynamic localization and interaction with other Bacillus subtilis actin-like proteins are important for the function of MreB. Mol Microbiol 62: 1340-1356
18. Domian IJ, Quon KC, Shapiro L (1997) Cell type-specific phosphor-ylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90: 415-424
19. Ebersbach G, Briegel A, Jensen GJ, Jacobs-Wagner C (2008) A self-associating protein critical for chromosome attachment, division, and polar organization in Caulobacter. Cell 134: 956-968
20. Edwards DH, Errington J (1997) The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24: 905-915
21. Edwards DH, Thomaides HB, Errington J (2000) Promiscuous targeting of Bacillus subtilis cell division protein DivIVA to division sites in Escherichia coli and fission yeast. EMBO J 19: 2719-2727
22. Ely B (1991) Genetics of Caulobacter crescentus. Methods Enzymol 204: 372-384
23. Esue O, Cordero M, Wirtz D, Tseng Y (2005) The assembly of MreB, a prokaryotic homolog of actin. J Biol Chem 280: 2628-2635
24. Evinger M, Agabian N (1977) Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol 132: 294-301
25. Finn RD, Tate J, Mistry J, Coggill PC, Sammut SJ, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucleic Acids Res 36: D281-D288
26. Flärdh K (2003) Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Mol Microbiol 49: 1523-1536
27. Frost A, Unger VM, De Camilli P (2009) The BAR domain super-family: membrane-molding macromolecules. Cell 137: 191-196
28. Fujiki Y, Hubbard AL, Fowler S, Lazarow PB (1982) Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol 93: 97-102
29. Gayda RC, Henk MC, Leong D (1992) C-shaped cells caused by expression of an ftsA mutation in Escherichia coli. J Bacteriol 174: 5362-5370
30. Gitai Z, Dye NA, Reisenauer A, Wachi M, Shapiro L (2005) MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120: 329-341
31. Goehring NW, Beckwith J (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15: R514-R526
32. Goldman BS, Nierman WC, Kaiser D, Slater SC, Durkin AS, Eisen JA, Ronning CM, Barbazuk WB, Blanchard M, Field C, Halling C, Hinkle G, Iartchuk O, Kim HS, Mackenzie C, Madupu R, Miller N, Shvartsbeyn A, Sullivan SA, Vaudin M et al (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci USA 103: 15200-15205
33. Gonin M, Quardokus EM, O'Donnol D, Maddock J, Brun YV (2000) Regulation of stalk elongation by phosphate in Caulobacter crescentus. J Bacteriol 182: 337-347
34. Graumann PL (2007) Cytoskeletal elements in bacteria. Annu Rev Microbiol 61: 589-618
35. Hay NA, Tipper DJ, Gygi D, Hughes C (1999) A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabilis. J Bacteriol 181: 2008-2016
36. Herrmann H, Aebi U (2004) Intermediate filaments: molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds. Annu Rev Biochem 73: 749-789
37. Hodgkin J, Kaiser D (1977) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci USA 74: 2938-2942
38. Hodgkin J, Kaiser D (1979) Genetics of gliding motility in Myxococcus xanthus (Myxobacterales)-2 gene systems control movement. Mol Gen Genet 171: 177-191 (Pubitemid 9247062)
39. Iancu CV, Tivol WF, Schooler JB, Dias DP, Henderson GP, Murphy GE, Wright ER, Li Z, Yu Z, Briegel A, Gan L, He Y, Jensen GJ (2006) Electron cryotomography sample preparation using the Vitrobot. Nat Protoc 1: 2813-2819
40. Iwai N, Nagai K, Wachi M (2002) Novel S-benzylisothiourea compound that induces spherical cells in Escherichia coli probably by acting on a rod-shape-determining protein(s) other than penicillin-binding protein 2. Biosci Biotechnol Biochem 66: 2658-2662
41. Izard J, Samsonoff WA, Kinoshita MB, Limberger RJ (1999) Genetic and structural analyses of cytoplasmic filaments of wild-type Treponema phagedenis and a flagellar filament-deficient mutant. J Bacteriol 181: 6739-6746
42. Jones LJ, Carballido-Lopez R, Errington J (2001) Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104: 913-922
43. Kahnt J, Buchenau B, Mahlert F, Kruger M, Shima S, Thauer RK (2007) Post-translational modifications in the active site region of methyl-coenzyme M reductase from methanogenic and methano-trophic archaea. FEBS J 274: 4913-4921
44. Kaiser D (1979) Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci USA 76: 5952-5956
45. Kashefi K, Hartzell PL (1995) Genetic suppression and phenotypic masking of a Myxococcus xanthus frzF-defect. Mol Microbiol 15: 483-494
46. Lenarcic R, Halbedel S, Visser L, Shaw M, Wu LJ, Errington J, Marenduzzo D, Hamoen LW (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28: 2272-2282
47. Letek M, Ordonez E, Vaquera J, Margolin W, Flardh K, Mateos LM, Gil JA (2008) DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J Bacteriol 190: 3283-3292
48. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23: 127-128
49. Li Z, Trimble MJ, Brun YV, Jensen GJ (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26: 4694-4708
50. Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120: 343-352
51. McGrath PT, Lee H, Zhang L, Iniesta AA, Hottes AK, Tan MH, Hillson NJ, Hu P, Shapiro L, McAdams HH (2007) High-throughput identification of transcription start sites, conserved promoter motifs and predicted regulons. Nat Biotechnol 25: 584-592
52. Meisenzahl AC, Shapiro L, Jenal U (1997) Isolation and characterization of a xylose-dependent promoter from Caulobacter crescentus. J Bacteriol 179: 592-600
53. Mukherjee A, Lutkenhaus J (1998) Dynamic assembly of FtsZ regulated by GTP hydrolysis. EMBO J 17: 462-469
54. Nierman WC, Feldblyum TV, Laub MT, Paulsen IT, Nelson KE, Eisen JA, Heidelberg JF, Alley MR, Ohta N, Maddock JR, Potocka I, Nelson WC, Newton A, Stephens C, Phadke ND, Ely B, DeBoy RT, Dodson RJ, Durkin AS, Gwinn ML et al (2001) Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci USA 98: 4136-4141
55. Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320: 792-794
56. Pogliano J (2008) The bacterial cytoskeleton. Curr Opin Cell Biol 20: 19-27
57. Poindexter JS, Hagenzieker JG (1982) Novel peptidoglycans in Caulobacter and Asticcacaulis spp. J Bacteriol 150: 332-347
58. Quardokus EM, Din N, Brun YV (2001) Cell cycle and positional constraints on FtsZ localization and the initiation of cell division in Caulobacter crescentus. Mol Microbiol 39: 949-959
59. Quon KC, Marczynski GT, Shapiro L (1996) Cell cycle control by an essential bacterial two-component signal transduction protein. Cell 84: 83-93
60. Radhakrishnan SK, Thanbichler M, Viollier PH (2008) The dynamic interplay between a cell fate determinant and a lyso-zyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes Dev 22: 212-225
61. Rajagopala SV, Titz B, Goll J, Parrish JR, Wohlbold K, McKevitt MT, Palzkill T, Mori H, Finley Jr RL, Uetz P (2007) The protein network of bacterial motility. Mol Syst Biol 3: 128
62. Ramamurthi KS, Losick R (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci USA 106: 13541-13545
63. Schmidt JM, Stanier RY (1966) The development of cellular stalks in bacteria. J Cell Biol 28: 423-436
64. Sogaard-Andersen L (2004) Cell polarity, intercellular signalling and morphogenetic cell movements in Myxococcus xanthus. Curr Opin Microbiol 7: 587-593
65. Stahlberg H, Kutejova E, Muchova K, Gregorini M, Lustig A, Muller SA, Olivieri V, Engel A, Wilkinson AJ, Barak I (2004) Oligomeric structure of the Bacillus subtilis cell division protein DivIVA determined by transmission electron microscopy. Mol Microbiol 52: 1281-1290
66. Suloway C, Shi J, Cheng A, Pulokas J, Carragher B, Potter CS, Zheng SQ, Agard DA, Jensen GJ (2009) Fully automated, sequential tilt-series acquisition with Leginon. J Struct Biol 167: 11-18
67. Thanbichler M, Iniesta AA, Shapiro L (2007) A comprehensive set of plasmids for vanillate-and xylose-inducible gene expression in Caulobacter crescentus. Nucleic Acids Res 35: e137
68. Thanbichler M, Shapiro L (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126: 147-162
69. Thanbichler M, Shapiro L (2008) Getting organized-how bacterial cells move proteins and DNA. Nat Rev Microbiol 6: 28-40
70. Tivol WF, Briegel A, Jensen GJ (2008) An improved cryogen for plunge freezing. Microsc Microanal 14: 375-379
71. Ueki T, Inouye S, Inouye M (1996) Positive-negative KG cassettes for construction of multi-gene deletions using a single drug marker. Gene 183: 153-157
72. Venkateswaran K, Moser DP, Dollhopf ME, Lies DP, Saffarini DA, MacGregor BJ, Ringelberg DB, White DC, Nishijima M, Sano H, Burghardt J, Stackebrandt E, Nealson KH (1999) Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov. Int J Syst Bacteriol 49: 705-724
73. Wheeler RT, Shapiro L (1999) Differential localization of two histidine kinases controlling bacterial cell differentiation. Mol Cell 4: 683-694
74. Williamson MP (1994) The structure and function of proline-rich regions in proteins. Biochem J 297: 249-260
75. Wu LJ, Errington J (2003) RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol Microbiol 49: 1463-1475
76. Wu SS, Wu J, Kaiser D (1997) The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol Microbiol 23: 109-121
77. Youderian P, Burke N, White DJ, Hartzell PL (2003) Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol Microbiol 49: 555-570
78. Youderian P, Hartzell PL (2006) Transposon insertions of magellan-4 that impair social gliding motility in Myxococcus xanthus. Genetics 172: 1397-1410
79. Zheng QS, Braunfeld MB, Sedat JW, Agard DA (2004) An improved strategy for automated electron microscopic tomography. J Struct Biol 147: 91-101