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c-di-GMP Arms an Anti-σ to Control Progression of Multicellular Differentiation in Streptomyces.

Publication ,  Journal Article
Gallagher, KA; Schumacher, MA; Bush, MJ; Bibb, MJ; Chandra, G; Holmes, NA; Zeng, W; Henderson, M; Zhang, H; Findlay, KC; Brennan, RG; Buttner, MJ
Published in: Mol Cell
February 6, 2020

Streptomyces are our primary source of antibiotics, produced concomitantly with the transition from vegetative growth to sporulation in a complex developmental life cycle. We previously showed that the signaling molecule c-di-GMP binds BldD, a master repressor, to control initiation of development. Here we demonstrate that c-di-GMP also intervenes later in development to control differentiation of the reproductive hyphae into spores by arming a novel anti-σ (RsiG) to bind and sequester a sporulation-specific σ factor (σWhiG). We present the structure of the RsiG-(c-di-GMP)2-σWhiG complex, revealing an unusual, partially intercalated c-di-GMP dimer bound at the RsiG-σWhiG interface. RsiG binds c-di-GMP in the absence of σWhiG, employing a novel E(X)3S(X)2R(X)3Q(X)3D motif repeated on each helix of a coiled coil. Further studies demonstrate that c-di-GMP is essential for RsiG to inhibit σWhiG. These findings reveal a newly described control mechanism for σ-anti-σ complex formation and establish c-di-GMP as the central integrator of Streptomyces development.

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Published In

Mol Cell

DOI

EISSN

1097-4164

Publication Date

February 6, 2020

Volume

77

Issue

3

Start / End Page

586 / 599.e6

Location

United States

Related Subject Headings

  • Streptomyces
  • Spores, Bacterial
  • Sigma Factor
  • RNA, Bacterial
  • Protein Domains
  • Gene Expression Regulation, Bacterial
  • Developmental Biology
  • DNA-Binding Proteins
  • Cyclic GMP
  • Bacterial Proteins
 

Citation

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Gallagher, K. A., Schumacher, M. A., Bush, M. J., Bibb, M. J., Chandra, G., Holmes, N. A., … Buttner, M. J. (2020). c-di-GMP Arms an Anti-σ to Control Progression of Multicellular Differentiation in Streptomyces. Mol Cell, 77(3), 586-599.e6. https://doi.org/10.1016/j.molcel.2019.11.006
Gallagher, Kelley A., Maria A. Schumacher, Matthew J. Bush, Maureen J. Bibb, Govind Chandra, Neil A. Holmes, Wenjie Zeng, et al. “c-di-GMP Arms an Anti-σ to Control Progression of Multicellular Differentiation in Streptomyces.Mol Cell 77, no. 3 (February 6, 2020): 586-599.e6. https://doi.org/10.1016/j.molcel.2019.11.006.
Gallagher KA, Schumacher MA, Bush MJ, Bibb MJ, Chandra G, Holmes NA, et al. c-di-GMP Arms an Anti-σ to Control Progression of Multicellular Differentiation in Streptomyces. Mol Cell. 2020 Feb 6;77(3):586-599.e6.
Gallagher, Kelley A., et al. “c-di-GMP Arms an Anti-σ to Control Progression of Multicellular Differentiation in Streptomyces.Mol Cell, vol. 77, no. 3, Feb. 2020, pp. 586-599.e6. Pubmed, doi:10.1016/j.molcel.2019.11.006.
Gallagher KA, Schumacher MA, Bush MJ, Bibb MJ, Chandra G, Holmes NA, Zeng W, Henderson M, Zhang H, Findlay KC, Brennan RG, Buttner MJ. c-di-GMP Arms an Anti-σ to Control Progression of Multicellular Differentiation in Streptomyces. Mol Cell. 2020 Feb 6;77(3):586-599.e6.
Journal cover image

Published In

Mol Cell

DOI

EISSN

1097-4164

Publication Date

February 6, 2020

Volume

77

Issue

3

Start / End Page

586 / 599.e6

Location

United States

Related Subject Headings

  • Streptomyces
  • Spores, Bacterial
  • Sigma Factor
  • RNA, Bacterial
  • Protein Domains
  • Gene Expression Regulation, Bacterial
  • Developmental Biology
  • DNA-Binding Proteins
  • Cyclic GMP
  • Bacterial Proteins