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Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae

Author

Listed:
  • Paula Yagüe

    (Área de Microbiología, Facultad de Medicina, Universidad de Oviedo)

  • Joost Willemse

    (Molecular Biotechnology, Institute of Biology, Leiden University)

  • Roman I. Koning

    (Leiden University Medical Centre)

  • Beatriz Rioseras

    (Área de Microbiología, Facultad de Medicina, Universidad de Oviedo)

  • María T. López-García

    (Área de Microbiología, Facultad de Medicina, Universidad de Oviedo)

  • Nathaly Gonzalez-Quiñonez

    (Área de Microbiología, Facultad de Medicina, Universidad de Oviedo)

  • Carmen Lopez-Iglesias

    (Crio-Microscòpia Electrònica. Centres Científics i Tecnològics, Universitat de Barcelona
    Present address: Nanoscopy Division of the Maastricht MultiModal Molecular Imaging Institute (M4i) Maastricht University, Maastricht 6211 LK, The Netherlands)

  • Pavel V. Shliaha

    (University of Southern Denmark)

  • Adelina Rogowska-Wrzesinska

    (University of Southern Denmark)

  • Abraham J. Koster

    (Leiden University Medical Centre)

  • Ole N. Jensen

    (University of Southern Denmark)

  • Gilles P. van Wezel

    (Molecular Biotechnology, Institute of Biology, Leiden University
    Microbial Ecology, Netherlands Institute for Ecology (NIOO-KNAW))

  • Ángel Manteca

    (Área de Microbiología, Facultad de Medicina, Universidad de Oviedo)

Abstract

Bacteria of the genus Streptomyces are a model system for bacterial multicellularity. Their mycelial life style involves the formation of long multinucleated hyphae during vegetative growth, with occasional cross-walls separating long compartments. Reproduction occurs by specialized aerial hyphae, which differentiate into chains of uninucleoid spores. While the tubulin-like FtsZ protein is required for the formation of all peptidoglycan-based septa in Streptomyces, canonical divisome-dependent cell division only occurs during sporulation. Here we report extensive subcompartmentalization in young vegetative hyphae of Streptomyces coelicolor, whereby 1 μm compartments are formed by nucleic acid stain-impermeable barriers. These barriers possess the permeability properties of membranes and at least some of them are cross-membranes without detectable peptidoglycan. Z-ladders form during the early growth, but cross-membrane formation does not depend on FtsZ. Thus, a new level of hyphal organization is presented involving unprecedented high-frequency compartmentalization, which changes the old dogma that Streptomyces vegetative hyphae have scarce compartmentalization.

Suggested Citation

  • Paula Yagüe & Joost Willemse & Roman I. Koning & Beatriz Rioseras & María T. López-García & Nathaly Gonzalez-Quiñonez & Carmen Lopez-Iglesias & Pavel V. Shliaha & Adelina Rogowska-Wrzesinska & Abraham, 2016. "Subcompartmentalization by cross-membranes during early growth of Streptomyces hyphae," Nature Communications, Nature, vol. 7(1), pages 1-11, November.
  • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12467
    DOI: 10.1038/ncomms12467
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