MreB-Dependent Inhibition of Cell Elongation during the Escape from Competence in Bacillus subtilis

PLoS Genetics

Volumn 11, Issue 6, 2015, Pages

  Mirouze, Nicolas ^a   Ferret, Cécile ^a   Yao, Zhizhong ^a   Chastanet, Arnaud ^a   Carballido López, Rut ^a  

^a UMR1319 MICALIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MREB PROTEIN; PROTEIN COMGA; PROTEIN MBL; PROTEIN MREBH; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; ISOPROTEIN;

ADAPTATION; ARTICLE; BACILLUS SUBTILIS; BACTERIAL GENE; BACTERIAL STRAIN; CELL ELONGATION; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FUSION; MBL GENE; MORPHOLOGY; MREB GENE; NONHUMAN; OPERON; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; REGULON; CELL CYCLE; CYTOLOGY; GENETIC TRANSFORMATION; GENETICS; METABOLISM;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CELL CYCLE; CYTOSKELETAL PROTEINS; DNA TRANSFORMATION COMPETENCE; PROTEIN ISOFORMS;

EID: 84937799156     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005299     Document Type: Article

References (76)

1. Dubnau D, Losick R, (2006) Bistability in bacteria. Mol Microbiol 61: 564–572. 16879639
2. Berka RM, Hahn J, Albano M, Draskovic I, Persuh M, et al. (2002) Microarray analysis of the Bacillus subtilis K-state: genome-wide expression changes dependent on ComK. Mol Microbiol 43: 1331–1345. 11918817
3. Fujita M, Gonzalez-Pastor JE, Losick R, (2005) High- and low-threshold genes in the Spo0A regulon of Bacillus subtilis. J Bacteriol 187: 1357–1368. 15687200
4. Hahn J, Maier B, Haijema BJ, Sheetz M, Dubnau D, (2005) Transformation proteins and DNA uptake localize to the cell poles in Bacillus subtilis. Cell 122: 59–71. 16009133
5. Higgins D, Dworkin J, (2012) Recent progress in Bacillus subtilis sporulation. FEMS Microbiol Rev 36: 131–148. doi: 10.1111/j.1574-6976.2011.00310.x 22091839
6. Ogura M, Yamaguchi H, Kobayashi K, Ogasawara N, Fujita Y, et al. (2002) Whole-genome analysis of genes regulated by the Bacillus subtilis competence transcription factor ComK. J Bacteriol 184: 2344–2351. 11948146
7. Hamoen LW, Smits WK, de Jong A, Holsappel S, Kuipers OP, (2002) Improving the predictive value of the competence transcription factor (ComK) binding site in Bacillus subtilis using a genomic approach. Nucleic Acids Res 30: 5517–5528. 12490720
8. Cahn FH, Fox MS, (1968) Fractionation of transformable bacteria from ocompetent cultures of Bacillus subtilis on renografin gradients. J Bacteriol 95: 867–875. 4966830
9. Hadden C, Nester EW, (1968) Purification of competent cells in the Bacillus subtilis transformation system. J Bacteriol 95: 876–885. 4966831
10. Hahn J, Albano M, Dubnau D, (1987) Isolation and characterization of Tn917lac-generated competence mutants of Bacillus subtilis. J Bacteriol 169: 3104–3109. 3036770
11. Haijema BJ, Hahn J, Haynes J, Dubnau D, (2001) A ComGA-dependent checkpoint limits growth during the escape from competence. Mol Microbiol 40: 52–64. 11298275
12. Briley K, Jr.Prepiak P, Dias MJ, Hahn J, Dubnau D, (2011) Maf acts downstream of ComGA to arrest cell division in competent cells of B. subtilis. Mol Microbiol 81: 23–39. doi: 10.1111/j.1365-2958.2011.07695.x 21564336
13. Kramer N, Hahn J, Dubnau D, (2007) Multiple interactions among the competence proteins of Bacillus subtilis. Mol Microbiol 65: 454–464. 17630974
14. Chastanet A, Carballido-López R, (2012) The actin-like MreB proteins in Bacillus subtilis: a new turn. Front Biosci (Schol Ed) 4: 1582–1606. 22652894
15. Carballido-López R, (2006) The bacterial actin-like cytoskeleton. Microbiol Mol Biol Rev 70: 888–909. 17158703
16. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Soldner R, et al. (2011) Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333: 225–228. doi: 10.1126/science.1203466 21636744
17. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, et al. (2011) Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333: 222–225. doi: 10.1126/science.1203285 21636745
18. Olshausen PV, Defeu Soufo HJ, Wicker K, Heintzmann R, Graumann PL, et al. (2013) Superresolution Imaging of Dynamic MreB Filaments in B. subtilis-A Multiple-Motor-Driven Transport? Biophys J 105: 1171–1181. doi: 10.1016/j.bpj.2013.07.038 24010660
19. Reimold C, Defeu Soufo HJ, Dempwolff F, Graumann PL, (2013) Motion of variable-length MreB filaments at the bacterial cell membrane influences cell morphology. Mol Biol Cell 24: 2340–2349. doi: 10.1091/mbc.E12-10-0728 23783036
20. Defeu Soufo HJ, Graumann PL, (2004) Dynamic movement of actin-like proteins within bacterial cells. EMBO Rep 5: 789–794. 15272301
21. van Teeffelen S, Wang S, Furchtgott L, Huang KC, Wingreen NS, et al. (2011) The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proc Natl Acad Sci U S A 108: 15822–15827. doi: 10.1073/pnas.1108999108 21903929
22. Kawai Y, Asai K, Errington J, (2009) Partial functional redundancy of MreB isoforms, MreB, Mbl and MreBH, in cell morphogenesis of Bacillus subtilis. Mol Microbiol 73: 719–731. doi: 10.1111/j.1365-2958.2009.06805.x 19659933
23. 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. 11290328
24. Schirner K, Errington J, (2009) Influence of heterologous MreB proteins on cell morphology of Bacillus subtilis. Microbiology 155: 3611–3621. doi: 10.1099/mic.0.030692-0 19643765
25. Carballido-López R, Formstone A, Li Y, Ehrlich SD, Noirot P, et al. (2006) Actin homolog MreBH governs cell morphogenesis by localization of the cell wall hydrolase LytE. Dev Cell 11: 399–409. 16950129
26. Nicolas P, Mäder U, Dervyn E, Rochat T, Leduc A, et al. (2012) Condition-Dependent Transcriptome Reveals High-Level Regulatory Architecture in Bacillus subtilis. Science 335: 1103–1106. doi: 10.1126/science.1206848 22383849
27. Eiamphungporn W, Helmann JD, (2008) The Bacillus subtilis sigma(M) regulon and its contribution to cell envelope stress responses. Mol Microbiol 67: 830–848. doi: 10.1111/j.1365-2958.2007.06090.x 18179421
28. Kunkel B, Kroos L, Poth H, Youngman P, Losick R, (1989) Temporal and spatial control of the mother-cell regulatory gene spoIIID of Bacillus subtilis. Genes Dev 3: 1735–1744. 2514119
29. Decatur A, McMurry MT, Kunkel BN, Losick R, (1997) Translation of the mRNA for the sporulation gene spoIIID of Bacillus subtilis is dependent upon translation of a small upstream open reading frame. J Bacteriol 179: 1324–1328. 9023218
30. Feucht A, Evans L, Errington J, (2003) Identification of sporulation genes by genome-wide analysis of the sigmaE regulon of Bacillus subtilis. Microbiology 149: 3023–3034. 14523133
31. Tseng CL, Shaw GC, (2008) Genetic evidence for the actin homolog gene mreBH and the bacitracin resistance gene bcrC as targets of the alternative sigma factor SigI of Bacillus subtilis. J Bacteriol 190: 1561–1567. 18156261
32. Turgay K, Hahn J, Burghoorn J, Dubnau D, (1998) Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor. EMBO J 17: 6730–6738. 9890793
33. Kong L, Siranosian KJ, Grossman AD, Dubnau D, (1993) Sequence and properties of mecA, a negative regulator of genetic competence in Bacillus subtilis. Mol Microbiol 9: 365–373. 8412687
34. Asai K, Yamaguchi H, Kang CM, Yoshida K, Fujita Y, et al. (2003) DNA microarray analysis of Bacillus subtilis sigma factors of extracytoplasmic function family. FEMS Microbiol Lett 220: 155–160. 12644242
35. Albano M, Hahn J, Dubnau D, (1987) Expression of competence genes in Bacillus subtilis. J Bacteriol 169: 3110–3117. 3110135
36. Eichenberger P, Fujita M, Jensen ST, Conlon EM, Rudner DZ, et al. (2004) The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol 2: e328. 15383836
37. Hahn J, Bylund J, Haines M, Higgins M, Dubnau D, (1995) Inactivation of mecA prevents recovery from the competent state and interferes with cell division and the partitioning of nucleoids in Bacillus subtilis. Mol Microbiol 18: 755–767. 8817496
38. Rashid MH, Tamakoshi A, Sekiguchi J, (1996) Effects of mecA and mecB (clpC) mutations on expression of sigD, which encodes an alternative sigma factor, and autolysin operons and on flagellin synthesis in Bacillus subtilis. J Bacteriol 178: 4861–4869. 8759849
39. Zeghouf M, Li J, Butland G, Borkowska A, Canadien V, et al. (2004) Sequential Peptide Affinity (SPA) system for the identification of mammalian and bacterial protein complexes. J Proteome Res 3: 463–468. 15253427
40. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, et al. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265–1272. 15958392
41. Formstone A, Errington J, (2005) A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis. Mol Microbiol 55: 1646–1657. 15752190
42. Schirner K, Errington J, (2009) The cell wall regulator {sigma}I specifically suppresses the lethal phenotype of mbl mutants in Bacillus subtilis. J Bacteriol 191: 1404–1413. doi: 10.1128/JB.01497-08 19114499
43. Bruckner A, Polge C, Lentze N, Auerbach D, Schlattner U, (2009) Yeast two-hybrid, a powerful tool for systems biology. Int J Mol Sci 10: 2763–2788. doi: 10.3390/ijms10062763 19582228
44. Kawai Y, Daniel RA, Errington J, (2009) Regulation of cell wall morphogenesis in Bacillus subtilis by recruitment of PBP1 to the MreB helix. Mol Microbiol 71: 1131–1144. doi: 10.1111/j.1365-2958.2009.06601.x 19192185
45. Dubnau D, (1997) Binding and transport of transforming DNA by Bacillus subtilis: the role of type-IV pilin-like proteins—a review. Gene 192: 191–198. 9224890
46. Jakutyte L, Baptista C, Sao-Jose C, Daugelavicius R, Carballido-Lopez R, et al. (2011) Bacteriophage infection in rod-shaped gram-positive bacteria: evidence for a preferential polar route for phage SPP1 entry in Bacillus subtilis. J Bacteriol 193: 4893–4903. doi: 10.1128/JB.05104-11 21705600
47. Sao-Jose C, Baptista C, Santos MA, (2004) Bacillus subtilis operon encoding a membrane receptor for bacteriophage SPP1. J Bacteriol 186: 8337–8346. 15576783
48. Abdallah AM, Gey van Pittius NC, Champion PA, Cox J, Luirink J, et al. (2007) Type VII secretion—mycobacteria show the way. Nat Rev Microbiol 5: 883–891. 17922044
49. Nilsen T, Yan AW, Gale G, Goldberg MB, (2005) Presence of multiple sites containing polar material in spherical Escherichia coli cells that lack MreB. J Bacteriol 187: 6187–6196. 16109960
50. Pradel N, Santini CL, Bernadac A, Shih YL, Goldberg MB, et al. (2007) Polar positional information in Escherichia coli spherical cells. Biochem Biophys Res Commun 353: 493–500. 17188233
51. Cowles KN, Gitai Z, (2010) Surface association and the MreB cytoskeleton regulate pilus production, localization and function in Pseudomonas aeruginosa. Mol Microbiol 76: 1411–1426. doi: 10.1111/j.1365-2958.2010.07132.x 20398206
52. Briley K, Jr.Dorsey-Oresto A, Prepiak P, Dias MJ, Mann JM, et al. (2011) The secretion ATPase ComGA is required for the binding and transport of transforming DNA. Mol Microbiol 81: 818–830. doi: 10.1111/j.1365-2958.2011.07730.x 21707789
53. Rudner DZ, Losick R, (2010) Protein subcellular localization in bacteria. Cold Spring Harb Perspect Biol 2: a000307. doi: 10.1101/cshperspect.a000307 20452938
54. Siripala AD, Welch MD, (2007) SnapShot: actin regulators II. Cell 128: 1014. 17350583
55. Siripala AD, Welch MD, (2007) SnapShot: actin regulators I. Cell 128: 626. 17289579
56. Schirner K, Eun YJ, Dion M, Luo Y, Helmann JD, et al. (2015) Lipid-linked cell wall precursors regulate membrane association of bacterial actin MreB. Nat Chem Biol 11: 38–45. doi: 10.1038/nchembio.1689 25402772
57. Lam H, Oh DC, Cava F, Takacs CN, Clardy J, et al. (2009) D-amino acids govern stationary phase cell wall remodeling in bacteria. Science 325: 1552–1555. doi: 10.1126/science.1178123 19762646
58. Hu Z, Mukherjee A, Pichoff S, Lutkenhaus J, (1999) The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci U S A 96: 14819–14824. 10611296
59. Gueiros-Filho FJ, Losick R, (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16: 2544–2556. 12368265
60. Romberg L, Levin PA, (2003) Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. Annu Rev Microbiol 57: 125–154. 14527275
61. Wu LJ, Errington J, (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915–925. 15210112
62. Haeusser DP, Schwartz RL, Smith AM, Oates ME, Levin PA, (2004) EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol Microbiol 52: 801–814. 15101985
63. Bendezu FO, Hale CA, Bernhardt TG, de Boer PA, (2009) RodZ (YfgA) is required for proper assembly of the MreB actin cytoskeleton and cell shape in E. coli. EMBO J 28: 193–204. doi: 10.1038/emboj.2008.264 19078962
64. Huang WZ, Wang JJ, Chen HJ, Chen JT, Shaw GC, (2013) The heat-inducible essential response regulator WalR positively regulates transcription of sigI, mreBH and lytE in Bacillus subtilis under heat stress. Res Microbiol 164: 998–1008. doi: 10.1016/j.resmic.2013.10.003 24125693
65. Saito H, Miura KI, (1963) Preparation of Transforming Deoxyribonucleic Acid by Phenol Treatment. Biochim Biophys Acta 72: 619–629. 14071565
66. Mirouze N, Prepiak P, Dubnau D, (2011) Fluctuations in spo0A transcription control rare developmental transitions in Bacillus subtilis. PLoS Genet 7: e1002048. doi: 10.1371/journal.pgen.1002048 21552330
67. Gibson DG, Young L, Chuang RY, Venter JC, Hutchison CA, 3rdet al. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343–345. doi: 10.1038/nmeth.1318 19363495
68. Mirouze N, Desai Y, Raj A, Dubnau D, (2012) Spo0A~P imposes a temporal gate for the bimodal expression of competence in Bacillus subtilis. PLoS Genet 8: e1002586. doi: 10.1371/journal.pgen.1002586 22412392
69. Fabret C, Ehrlich SD, Noirot P, (2002) A new mutation delivery system for genome-scale approaches in Bacillus subtilis. Mol Microbiol 46: 25–36. 12366828
70. Guerout-Fleury AM, Frandsen N, Stragier P, (1996) Plasmids for ectopic integration in Bacillus subtilis. Gene 180: 57–61. 8973347
71. Kearns DB, Losick R, (2005) Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev 19: 3083–3094. 16357223
72. Lewis PJ, Marston AL, (1999) GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227: 101–110. 9931458
73. Rueff AS, Chastanet A, Dominguez-Escobar J, Yao Z, Yates J, et al. (2014) An early cytoplasmic step of peptidoglycan synthesis is associated to MreB in Bacillus subtilis. Mol Microbiol 91: 348–362. doi: 10.1111/mmi.12467 24261876
74. Hahn J, Luttinger A, Dubnau D, (1996) Regulatory inputs for the synthesis of ComK, the competence transcription factor of Bacillus subtilis. Mol Microbiol 21: 763–775. 8878039
75. Delumeau O, Lecointe F, Muntel J, Guillot A, Guedon E, et al. (2011) The dynamic protein partnership of RNA polymerase in Bacillus subtilis. Proteomics 11: 2992–3001. doi: 10.1002/pmic.201000790 21710567
76. Marchadier E, Carballido-Lopez R, Brinster S, Fabret C, Mervelet P, et al. (2011) An expanded protein-protein interaction network in Bacillus subtilis reveals a group of hubs: Exploration by an integrative approach. Proteomics 11: 2981–2991. doi: 10.1002/pmic.201000791 21630458