Literature DB >> 16484182

Developmental control of a parAB promoter leads to formation of sporulation-associated ParB complexes in Streptomyces coelicolor.

Dagmara Jakimowicz1, Sebastien Mouz, Jolanta Zakrzewska-Czerwinska, Keith F Chater.   

Abstract

The Streptomyces coelicolor partitioning protein ParB binds to numerous parS sites in the oriC-proximal part of the linear chromosome. ParB binding results in the formation of large complexes, which behave differentially during the complex life cycle (D. Jakimowicz, B. Gust, J. Zakrzewska-Czerwinska, and K. F. Chater, J. Bacteriol. 187:3572-3580, 2005). Here we have analyzed the transcriptional regulation that underpins this developmentally specific behavior. Analysis of promoter mutations showed that the irregularly spaced complexes present in vegetative hyphae are dependent on the constitutive parABp(1) promoter, while sporulation-specific induction of the promoter parABp(2) is required for the assembly of arrays of ParB complexes in aerial hyphae and thus is necessary for efficient chromosome segregation. Expression from parABp(2) depended absolutely on two sporulation regulatory genes, whiA and whiB, and partially on two others, whiH and whiI, all four of which are needed for sporulation septation. Because of this pattern of dependence, we investigated the transcription of these four whi genes in whiA and whiB mutants, revealing significant regulatory interplay between whiA and whiB. A strain in which sporulation septation (but not vegetative septation) was blocked by mutation of a sporulation-specific promoter of ftsZ showed close to wild-type induction of parABp(2) and formed fairly regular ParB-enhanced green fluorescent protein foci in aerial hyphae, ruling out strong morphological coupling or checkpoint regulation between septation and DNA partitioning during sporulation. A model for developmental regulation of parABp(2) expression is presented.

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Year:  2006        PMID: 16484182      PMCID: PMC1426544          DOI: 10.1128/JB.188.5.1710-1720.2006

Source DB:  PubMed          Journal:  J Bacteriol        ISSN: 0021-9193            Impact factor:   3.490


  49 in total

Review 1.  Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex?

Authors:  K F Chater
Journal:  Curr Opin Microbiol       Date:  2001-12       Impact factor: 7.934

2.  Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2).

Authors:  M S Paget; L Chamberlin; A Atrih; S J Foster; M J Buttner
Journal:  J Bacteriol       Date:  1999-01       Impact factor: 3.490

3.  Identification and characterization of a bacterial chromosome partitioning site.

Authors:  D C Lin; A D Grossman
Journal:  Cell       Date:  1998-03-06       Impact factor: 41.582

4.  A connection between stress and development in the multicellular prokaryote Streptomyces coelicolor A3(2).

Authors:  G H Kelemen; P H Viollier; J Tenor; L Marri; M J Buttner; C J Thompson
Journal:  Mol Microbiol       Date:  2001-05       Impact factor: 3.501

5.  The chromosome partitioning protein, ParB, is required for cytokinesis in Caulobacter crescentus.

Authors:  D A Mohl; J Easter; J W Gober
Journal:  Mol Microbiol       Date:  2001-11       Impact factor: 3.501

Review 6.  The bacterial ParA-ParB partitioning proteins.

Authors:  C Bignell; C M Thomas
Journal:  J Biotechnol       Date:  2001-09-13       Impact factor: 3.307

7.  Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites.

Authors:  S Omura; H Ikeda; J Ishikawa; A Hanamoto; C Takahashi; M Shinose; Y Takahashi; H Horikawa; H Nakazawa; T Osonoe; H Kikuchi; T Shiba; Y Sakaki; M Hattori
Journal:  Proc Natl Acad Sci U S A       Date:  2001-09-25       Impact factor: 11.205

8.  Chromosome loss from par mutants of Pseudomonas putida depends on growth medium and phase of growth.

Authors:  Richard A Lewis; Colin R Bignell; Wei Zeng; Anthony C Jones; Christopher M Thomas
Journal:  Microbiology       Date:  2002-02       Impact factor: 2.777

9.  A developmentally regulated gene encoding a repressor-like protein is essential for sporulation in Streptomyces coelicolor A3(2).

Authors:  N J Ryding; G H Kelemen; C A Whatling; K Flärdh; M J Buttner; K F Chater
Journal:  Mol Microbiol       Date:  1998-07       Impact factor: 3.501

10.  Direct evidence for active segregation of oriC regions of the Bacillus subtilis chromosome and co-localization with the SpoOJ partitioning protein.

Authors:  P J Lewis; J Errington
Journal:  Mol Microbiol       Date:  1997-09       Impact factor: 3.501

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  24 in total

1.  Extended function of plasmid partition genes: the Sop system of linear phage-plasmid N15 facilitates late gene expression.

Authors:  Nikolai V Ravin; Jérôme Rech; David Lane
Journal:  J Bacteriol       Date:  2008-03-21       Impact factor: 3.490

Review 2.  Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium.

Authors:  Klas Flärdh; Mark J Buttner
Journal:  Nat Rev Microbiol       Date:  2009-01       Impact factor: 60.633

Review 3.  Compaction and control-the role of chromosome-organizing proteins in Streptomyces.

Authors:  Marcin J Szafran; Dagmara Jakimowicz; Marie A Elliot
Journal:  FEMS Microbiol Rev       Date:  2020-11-24       Impact factor: 16.408

4.  A Type Ib ParB protein involved in plasmid partitioning in a gram-positive bacterium.

Authors:  Ping Yin; Tai-Yuan Li; Mao-Hua Xie; Lina Jiang; Yi Zhang
Journal:  J Bacteriol       Date:  2006-09-22       Impact factor: 3.490

Review 5.  Signals and regulators that govern Streptomyces development.

Authors:  Joseph R McCormick; Klas Flärdh
Journal:  FEMS Microbiol Rev       Date:  2011-12-02       Impact factor: 16.408

6.  The conserved DNA-binding protein WhiA is involved in cell division in Bacillus subtilis.

Authors:  Katarina Surdova; Pamela Gamba; Dennis Claessen; Tjalling Siersma; Martijs J Jonker; Jeff Errington; Leendert W Hamoen
Journal:  J Bacteriol       Date:  2013-10-04       Impact factor: 3.490

7.  One of the two genes encoding nucleoid-associated HU proteins in Streptomyces coelicolor is developmentally regulated and specifically involved in spore maturation.

Authors:  Paola Salerno; Jessica Larsson; Giselda Bucca; Emma Laing; Colin P Smith; Klas Flärdh
Journal:  J Bacteriol       Date:  2009-08-28       Impact factor: 3.490

8.  Topoisomerase I (TopA) is recruited to ParB complexes and is required for proper chromosome organization during Streptomyces coelicolor sporulation.

Authors:  Marcin Szafran; Patrycja Skut; Bartosz Ditkowski; Katarzyna Ginda; Govind Chandra; Jolanta Zakrzewska-Czerwińska; Dagmara Jakimowicz
Journal:  J Bacteriol       Date:  2013-08-02       Impact factor: 3.490

9.  SMC protein-dependent chromosome condensation during aerial hyphal development in Streptomyces.

Authors:  Agnieszka Kois; Magdalena Swiatek; Dagmara Jakimowicz; Jolanta Zakrzewska-Czerwińska
Journal:  J Bacteriol       Date:  2008-10-17       Impact factor: 3.490

10.  cmdABCDEF, a cluster of genes encoding membrane proteins for differentiation and antibiotic production in Streptomyces coelicolor A3(2).

Authors:  Pengfei Xie; Ana Zeng; Zhongjun Qin
Journal:  BMC Microbiol       Date:  2009-08-04       Impact factor: 3.605

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