Literature DB >> 21505418

Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE.

Jutta Vogelmann1, Moritz Ammelburg, Constanze Finger, Jamil Guezguez, Dirk Linke, Matthias Flötenmeyer, York-Dieter Stierhof, Wolfgang Wohlleben, Günther Muth.   

Abstract

Conjugation is a major route of horizontal gene transfer, the driving force in the evolution of bacterial genomes. Antibiotic producing soil bacteria of the genus Streptomyces transfer DNA in a unique process involving a single plasmid-encoded protein TraB and a double-stranded DNA molecule. However, the molecular function of TraB in directing DNA transfer from a donor into a recipient cell is unknown. Here, we show that TraB constitutes a novel conjugation system that is clearly distinguished from DNA transfer by a type IV secretion system. We demonstrate that TraB specifically recognizes and binds to repeated 8 bp motifs on the conjugative plasmid. The specific DNA recognition is mediated by helix α3 of the C-terminal winged-helix-turn-helix domain of TraB. We show that TraB assembles to a hexameric ring structure with a central ∼3.1 nm channel and forms pores in lipid bilayers. Structure, sequence similarity and DNA binding characteristics of TraB indicate that TraB is derived from an FtsK-like ancestor protein, suggesting that Streptomyces adapted the FtsK/SpoIIIE chromosome segregation system to transfer DNA between two distinct Streptomyces cells.

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Year:  2011        PMID: 21505418      PMCID: PMC3117642          DOI: 10.1038/emboj.2011.121

Source DB:  PubMed          Journal:  EMBO J        ISSN: 0261-4189            Impact factor:   11.598


  44 in total

1.  The Protein Data Bank.

Authors:  H M Berman; J Westbrook; Z Feng; G Gilliland; T N Bhat; H Weissig; I N Shindyalov; P E Bourne
Journal:  Nucleic Acids Res       Date:  2000-01-01       Impact factor: 16.971

2.  EMAN: semiautomated software for high-resolution single-particle reconstructions.

Authors:  S J Ludtke; P R Baldwin; W Chiu
Journal:  J Struct Biol       Date:  1999-12-01       Impact factor: 2.867

3.  Modular architecture of the conjugative plasmid pSVH1 from Streptomyces venezuelae.

Authors:  Jens Reuther; Wolfgang Wohlleben; Günther Muth
Journal:  Plasmid       Date:  2006-01-24       Impact factor: 3.466

4.  Fully efficient chromosome dimer resolution in Escherichia coli cells lacking the integral membrane domain of FtsK.

Authors:  Nelly Dubarry; François-Xavier Barre
Journal:  EMBO J       Date:  2009-12-24       Impact factor: 11.598

Review 5.  Inactivation of antibiotics and the dissemination of resistance genes.

Authors:  J Davies
Journal:  Science       Date:  1994-04-15       Impact factor: 47.728

6.  Direct repeat sequences are essential for function of the cis-acting locus of transfer (clt) of Streptomyces phaeochromogenes plasmid pJV1.

Authors:  Bernardo Franco; Gabriela González-Cerón; Luis Servín-González
Journal:  Plasmid       Date:  2003-11       Impact factor: 3.466

7.  pIJ101, a multi-copy broad host-range Streptomyces plasmid: functional analysis and development of DNA cloning vectors.

Authors:  T Kieser; D A Hopwood; H M Wright; C J Thompson
Journal:  Mol Gen Genet       Date:  1982

8.  Sensory electrophysiology of bacteria: relationship of the membrane potential to motility and chemotaxis in Bacillus subtilis.

Authors:  J B Miller; D E Koshland
Journal:  Proc Natl Acad Sci U S A       Date:  1977-11       Impact factor: 11.205

9.  The FtsK gamma domain directs oriented DNA translocation by interacting with KOPS.

Authors:  Viknesh Sivanathan; Mark D Allen; Charissa de Bekker; Rachel Baker; Lidia K Arciszewska; Stefan M Freund; Mark Bycroft; Jan Löwe; David J Sherratt
Journal:  Nat Struct Mol Biol       Date:  2006-10-22       Impact factor: 15.369

10.  Structure of the outer membrane complex of a type IV secretion system.

Authors:  Vidya Chandran; Rémi Fronzes; Stéphane Duquerroy; Nora Cronin; Jorge Navaza; Gabriel Waksman
Journal:  Nature       Date:  2009-11-29       Impact factor: 49.962

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  28 in total

1.  A septal chromosome segregator protein evolved into a conjugative DNA-translocator protein.

Authors:  Edgardo Sepulveda; Jutta Vogelmann; Günther Muth
Journal:  Mob Genet Elements       Date:  2011-09-01

Review 2.  How hyperthermophiles adapt to change their lives: DNA exchange in extreme conditions.

Authors:  Marleen van Wolferen; Małgorzata Ajon; Arnold J M Driessen; Sonja-Verena Albers
Journal:  Extremophiles       Date:  2013-05-28       Impact factor: 2.395

3.  The FtsK-like motor TraB is a DNA-dependent ATPase that forms higher-order assemblies.

Authors:  Eric Amado; Günther Muth; Ignacio Arechaga; Elena Cabezón
Journal:  J Biol Chem       Date:  2019-02-05       Impact factor: 5.157

4.  The hexameric structure of a conjugative VirB4 protein ATPase provides new insights for a functional and phylogenetic relationship with DNA translocases.

Authors:  Alejandro Peña; Inmaculada Matilla; Jaime Martín-Benito; José M Valpuesta; José L Carrascosa; Fernando de la Cruz; Elena Cabezón; Ignacio Arechaga
Journal:  J Biol Chem       Date:  2012-10-03       Impact factor: 5.157

5.  High-salt stress conditions increase the pAW63 transfer frequency in Bacillus thuringiensis.

Authors:  Elise Beuls; Pauline Modrie; Cédric Deserranno; Jacques Mahillon
Journal:  Appl Environ Microbiol       Date:  2012-07-20       Impact factor: 4.792

6.  SpoIIIE mechanism of directional translocation involves target search coupled to sequence-dependent motor stimulation.

Authors:  Diego I Cattoni; Osvaldo Chara; Cédric Godefroy; Emmanuel Margeat; Sonia Trigueros; Pierre-Emmanuel Milhiet; Marcelo Nöllmann
Journal:  EMBO Rep       Date:  2013-04-05       Impact factor: 8.807

7.  Noncanonical cell-to-cell DNA transfer in Thermus spp. is insensitive to argonaute-mediated interference.

Authors:  Alba Blesa; Carolina Elvira César; Beate Averhoff; José Berenguer
Journal:  J Bacteriol       Date:  2014-10-20       Impact factor: 3.490

Review 8.  Blending genomes: distributive conjugal transfer in mycobacteria, a sexier form of HGT.

Authors:  Todd A Gray; Keith M Derbyshire
Journal:  Mol Microbiol       Date:  2018-05-11       Impact factor: 3.501

Review 9.  Molecular motors for DNA translocation in prokaryotes.

Authors:  Jean-François Allemand; Berenike Maier; Douglas E Smith
Journal:  Curr Opin Biotechnol       Date:  2012-01-07       Impact factor: 9.740

10.  Distributive Conjugal Transfer: New Insights into Horizontal Gene Transfer and Genetic Exchange in Mycobacteria.

Authors:  Keith M Derbyshire; Todd A Gray
Journal:  Microbiol Spectr       Date:  2014
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