Literature DB >> 21205868

Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces.

Joost Willemse1, Jan Willem Borst, Ellen de Waal, Ton Bisseling, Gilles P van Wezel.   

Abstract

In bacteria that divide by binary fission, cell division starts with the polymerization of the tubulin homolog FtsZ at mid-cell to form a cell division scaffold (the Z ring), followed by recruitment of the other divisome components. The current view of bacterial cell division control starts from the principle of negative checkpoints that prevent incorrect Z-ring positioning. Here we provide evidence of positive control of cell division during sporulation of Streptomyces, via the direct recruitment of FtsZ by the membrane-associated divisome component SsgB. In vitro studies demonstrated that SsgB promotes the polymerization of FtsZ. The interactions are shown in vivo by time-lapse imaging and Förster resonance energy transfer and fluorescence lifetime imaging microscopy (FRET-FLIM), and are corroborated independently via two-hybrid studies. As determined by fluorescence recovery after photobleaching (FRAP), the turnover of FtsZ protofilaments increased strongly at the time of Z-ring formation. The surprising positive control of Z-ring formation by SsgB implies the evolution of an entirely new way of Z-ring control, which may be explained by the absence of a mid-cell reference point in the long multinucleoid hyphae. In turn, the localization of SsgB is mediated through the orthologous SsgA, and premature expression of the latter is sufficient to directly activate multiple Z-ring formation and hyperdivision at early stages of the Streptomyces cell cycle.

Mesh:

Substances:

Year:  2011        PMID: 21205868      PMCID: PMC3012939          DOI: 10.1101/gad.600211

Source DB:  PubMed          Journal:  Genes Dev        ISSN: 0890-9369            Impact factor:   11.361


  54 in total

1.  Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET.

Authors:  Svetlana Alexeeva; Theodorus W J Gadella; Jolanda Verheul; Gertjan S Verhoeven; Tanneke den Blaauwen
Journal:  Mol Microbiol       Date:  2010-05-19       Impact factor: 3.501

2.  FtsZ ring structure associated with division in Escherichia coli.

Authors:  E F Bi; J Lutkenhaus
Journal:  Nature       Date:  1991-11-14       Impact factor: 49.962

3.  The MinE ring: an FtsZ-independent cell structure required for selection of the correct division site in E. coli.

Authors:  D M Raskin; P A de Boer
Journal:  Cell       Date:  1997-11-28       Impact factor: 41.582

4.  Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli.

Authors:  C A Hale; P A de Boer
Journal:  Cell       Date:  1997-01-24       Impact factor: 41.582

5.  Inactivation of FtsI inhibits constriction of the FtsZ cytokinetic ring and delays the assembly of FtsZ rings at potential division sites.

Authors:  J Pogliano; K Pogliano; D S Weiss; R Losick; J Beckwith
Journal:  Proc Natl Acad Sci U S A       Date:  1997-01-21       Impact factor: 11.205

6.  Septation during sporulation in Streptomyces coelicolor.

Authors:  H Wildermuth; D A Hopwood
Journal:  J Gen Microbiol       Date:  1970-01

7.  Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor.

Authors:  J Schwedock; J R McCormick; E R Angert; J R Nodwell; R Losick
Journal:  Mol Microbiol       Date:  1997-09       Impact factor: 3.501

8.  Cell division gene ftsQ is required for efficient sporulation but not growth and viability in Streptomyces coelicolor A3(2).

Authors:  J R McCormick; R Losick
Journal:  J Bacteriol       Date:  1996-09       Impact factor: 3.490

9.  Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ.

Authors:  J R McCormick; E P Su; A Driks; R Losick
Journal:  Mol Microbiol       Date:  1994-10       Impact factor: 3.501

10.  Spindle microtubule dynamics in sea urchin embryos: analysis using a fluorescein-labeled tubulin and measurements of fluorescence redistribution after laser photobleaching.

Authors:  E D Salmon; R J Leslie; W M Saxton; M L Karow; J R McIntosh
Journal:  J Cell Biol       Date:  1984-12       Impact factor: 10.539

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  77 in total

1.  An orphan histidine kinase, OhkA, regulates both secondary metabolism and morphological differentiation in Streptomyces coelicolor.

Authors:  Yinhua Lu; Juanmei He; Hong Zhu; Zhenyu Yu; Rui Wang; Yunliang Chen; Fujun Dang; Weiwen Zhang; Sheng Yang; Weihong Jiang
Journal:  J Bacteriol       Date:  2011-04-22       Impact factor: 3.490

Review 2.  Nucleoid occlusion and bacterial cell division.

Authors:  Ling Juan Wu; Jeff Errington
Journal:  Nat Rev Microbiol       Date:  2011-10-24       Impact factor: 60.633

Review 3.  The bacterial divisome: ready for its close-up.

Authors:  Veronica W Rowlett; William Margolin
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-10-05       Impact factor: 6.237

Review 4.  Taxonomy, Physiology, and Natural Products of Actinobacteria.

Authors:  Essaid Ait Barka; Parul Vatsa; Lisa Sanchez; Nathalie Gaveau-Vaillant; Cedric Jacquard; Jan P Meier-Kolthoff; Hans-Peter Klenk; Christophe Clément; Yder Ouhdouch; Gilles P van Wezel
Journal:  Microbiol Mol Biol Rev       Date:  2015-11-25       Impact factor: 11.056

5.  A conserved cell division protein directly regulates FtsZ dynamics in filamentous and unicellular actinobacteria.

Authors:  Félix Ramos-León; Matthew J Bush; Joseph W Sallmen; Govind Chandra; Jake Richardson; Kim C Findlay; Joseph R McCormick; Susan Schlimpert
Journal:  Elife       Date:  2021-03-17       Impact factor: 8.140

Review 6.  Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies.

Authors:  Dennis Claessen; Daniel E Rozen; Oscar P Kuipers; Lotte Søgaard-Andersen; Gilles P van Wezel
Journal:  Nat Rev Microbiol       Date:  2014-01-02       Impact factor: 60.633

Review 7.  Multidimensional view of the bacterial cytoskeleton.

Authors:  Katherine Celler; Roman I Koning; Abraham J Koster; Gilles P van Wezel
Journal:  J Bacteriol       Date:  2013-02-15       Impact factor: 3.490

8.  Regulation of Sporangium Formation by BldD in the Rare Actinomycete Actinoplanes missouriensis.

Authors:  Yoshihiro Mouri; Kenji Konishi; Azusa Fujita; Takeaki Tezuka; Yasuo Ohnishi
Journal:  J Bacteriol       Date:  2017-05-25       Impact factor: 3.490

Review 9.  FtsZ ring stability: of bundles, tubules, crosslinks, and curves.

Authors:  Kuo-Hsiang Huang; Jorge Durand-Heredia; Anuradha Janakiraman
Journal:  J Bacteriol       Date:  2013-03-01       Impact factor: 3.490

Review 10.  Pre-sporulation stages of Streptomyces differentiation: state-of-the-art and future perspectives.

Authors:  Paula Yagüe; Maria T López-García; Beatriz Rioseras; Jesús Sánchez; Angel Manteca
Journal:  FEMS Microbiol Lett       Date:  2013-04-12       Impact factor: 2.742

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