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Actin-like Proteins MreB and Mbl from Bacillus subtilis Are Required for Bipolar Positioning of Replication Origins

2003; Elsevier BV; Volume: 13; Issue: 21 Linguagem: Inglês

10.1016/j.cub.2003.10.024

1879-0445

Hervé Joël Defeu Soufo, Peter L. Graumann,

Genomics and Phylogenetic Studies

Actin-like proteins MreB and Mbl are required for proper cell shape and for viability in B. subtilis[1Jones L.J. Carballido-Lopez R. Errington J. Control of cell shape in bacteria helical, actin-like filaments in Bacillus subtilis.Cell. 2001; 104: 913-922Abstract Full Text Full Text PDF PubMed Scopus (710) Google Scholar, 2Abhayawardhane Y. Stewart G.C. Bacillus subtilis possesses a second determinant with extensive sequence similarity to the Escherichia coli mreB morphogene.J. Bacteriol. 1995; 177: 765-773PubMed Google Scholar] and form dynamic helical filaments underneath the cell membrane [1Jones L.J. Carballido-Lopez R. Errington J. Control of cell shape in bacteria helical, actin-like filaments in Bacillus subtilis.Cell. 2001; 104: 913-922Abstract Full Text Full Text PDF PubMed Scopus (710) Google Scholar, 3Carballido-Lopez R. Errington J. The bacterial cytoskeleton in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis.Dev. Cell. 2003; 4: 19-28Abstract Full Text Full Text PDF PubMed Scopus (149) Google Scholar]. We have found that depletion of MreB and Mbl proteins leads to a rapid defect in chromosome segregation before a defect in cell shape becomes detectable. Under these conditions, the SMC chromosome segregation complex that is essential for proper chromosome arrangement and segregation [4Mascarenhas J. Soppa J. Strunnikov A. Grauman P.L. Cell cycle dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein.EMBO J. 2002; 21: 3108-3118Crossref PubMed Scopus (133) Google Scholar, 5Britton R.A. Lin D.C. Grossman A.D. Characterization of a prokaryotic SMC protein involved in chromosome partitioning.Genes Dev. 1998; 12: 1254-1259Crossref PubMed Scopus (238) Google Scholar, 6Volkov A.V. Mascarenhas J. Andrei-Selmer C. Ulrich H.D. Grauman P.L. A prokaryotic condensin/cohesin-like complex can actively compact chromosomes from a single position on the nucleoid.Mol. Cell. Biol. 2003; 23: 5638-5650Crossref PubMed Scopus (84) Google Scholar] loses its specific subcellular localization, and replication origins fail to localize in a regular bipolar manner as in wild type cells [7Glaser P. Sharpe M.E. Raether B. Perego M. Ohlsen K. Errington J. Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning.Genes Dev. 1997; 11: 1160-1168Crossref PubMed Scopus (270) Google Scholar, 8Webb C.D. Teleman A. Gordon S. Straight A. Belmont A. Lin D.C.-H. Grossman A.D. Wright A. Losick R. Bipolar localization of the replication origin regions of chromosomes in vegetative and sporulating cells of B. subtilis.Cell. 1997; 88: 667-674Abstract Full Text Full Text PDF PubMed Scopus (305) Google Scholar, 9Webb C.D. Graumann P.L. Kahana J. Teleman A.A. Silver P. Losick R. Use of time-lapse microscopy to visualize rapid movement of the replication origin region of the chromosome during the cell cycle in Bacillus subtilis.Mol. Microbiol. 1998; 28: 883-892Crossref PubMed Scopus (170) Google Scholar, 10Teleman A.A. Graumann P.L. Lin D.C.H. Grossman A.D. Losick R. Chromosome arrangement within a bacterium.Curr. Biol. 1998; 8: 1102-1109Abstract Full Text Full Text PDF PubMed Scopus (164) Google Scholar]. Time-lapse microscopy showed that during depletion of MreB, origin regions can move towards the same cell pole, showing that bipolar orientation of origin separation is lost. Contrarily, depletion of three other cell shape determinants, MreC, MreD, or MreBH (the third B. subtilis actin homolog) had no effect on chromosome segregation but varying effects on cell morphology. Depletion of MreC and MreD resulted in formation of round cells, while depletion of MreBH led to formation of vibrio-shaped cells. The data show that actin proteins Mbl and MreB are required for proper chromosome segregation and that Mre proteins affect different aspects in cell shape.