1. Cell Biology
  2. Microbiology and Infectious Disease
Download icon

Coupling chemosensory array formation and localization

  1. Alejandra Alvarado
  2. Andreas Kjær
  3. Wen Yang
  4. Petra Mann
  5. Ariane Briegel
  6. Matthew K Waldor
  7. Simon Ringgaard  Is a corresponding author
  1. Max Planck Institute for Terrestrial Microbiology, Germany
  2. Leiden University, Netherlands
  3. Brigham and Women's Hospital, United States
Research Article
  • Cited 14
  • Views 1,557
  • Annotations
Cite this article as: eLife 2017;6:e31058 doi: 10.7554/eLife.31058

Abstract

Chemotaxis proteins organize into large, highly ordered, chemotactic signaling arrays, which in Vibrio species are found at the cell pole. Proper localization of signaling arrays is mediated by ParP, which tethers arrays to a cell pole anchor, ParC. Here we show that ParP's C-terminus integrates into the core-unit of signaling arrays through interactions with MCP-proteins and CheA. Its intercalation within core-units stimulates array formation, whereas its N-terminal interaction domain enables polar recruitment of arrays and facilitates its own polar localization. Linkage of these domains within ParP couples array formation and localization and results in controlled array positioning at the cell pole. Notably, ParP's integration into arrays modifies its own and ParC's subcellular localization dynamics, promoting their polar retention. ParP serves as a critical nexus that regulates the localization dynamics of its network constituents and drives the localized assembly and stability of the chemotactic machinery, resulting in proper cell pole development.

Article and author information

Author details

  1. Alejandra Alvarado

    Department for Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Andreas Kjær

    Department for Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Wen Yang

    Institute of Biology, Leiden University, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Petra Mann

    Department for Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Ariane Briegel

    Institute of Biology, Leiden University, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Matthew K Waldor

    Division of Infectious Diseases, Brigham and Women's Hospital, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1843-7000
  7. Simon Ringgaard

    Department for Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    For correspondence
    simon.ringgaard@mpi-marburg.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4980-5964

Funding

Max-Planck-Institut für Terrestrische Mikrobiologie (Open-access funding)

  • Simon Ringgaard

Deutsche Forschungsgemeinschaft (RI 2820/1-1)

  • Simon Ringgaard

National Institutes of Health (NIH R37 AI-042347)

  • Matthew K Waldor

Howard Hughes Medical Institute

  • Matthew K Waldor

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Tâm Mignot, Aix Marseille University-CNRS UMR7283, France

Publication history

  1. Received: August 5, 2017
  2. Accepted: October 22, 2017
  3. Accepted Manuscript published: October 23, 2017 (version 1)
  4. Version of Record published: November 29, 2017 (version 2)

Copyright

© 2017, Alvarado et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,557
    Page views
  • 312
    Downloads
  • 14
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Download citations (links to download the citations from this article in formats compatible with various reference manager tools)

Open citations (links to open the citations from this article in various online reference manager services)

Further reading

    1. Cell Biology
    2. Plant Biology
    Madlen Stephani et al.
    Research Article Updated

    Eukaryotes have evolved various quality control mechanisms to promote proteostasis in the endoplasmic reticulum (ER). Selective removal of certain ER domains via autophagy (termed as ER-phagy) has emerged as a major quality control mechanism. However, the degree to which ER-phagy is employed by other branches of ER-quality control remains largely elusive. Here, we identify a cytosolic protein, C53, that is specifically recruited to autophagosomes during ER-stress, in both plant and mammalian cells. C53 interacts with ATG8 via a distinct binding epitope, featuring a shuffled ATG8 interacting motif (sAIM). C53 senses proteotoxic stress in the ER lumen by forming a tripartite receptor complex with the ER-associated ufmylation ligase UFL1 and its membrane adaptor DDRGK1. The C53/UFL1/DDRGK1 receptor complex is activated by stalled ribosomes and induces the degradation of internal or passenger proteins in the ER. Consistently, the C53 receptor complex and ufmylation mutants are highly susceptible to ER stress. Thus, C53 forms an ancient quality control pathway that bridges selective autophagy with ribosome-associated quality control in the ER.

    1. Cell Biology
    2. Chromosomes and Gene Expression
    Maximilian H Fitz-James et al.
    Research Article Updated

    During mitosis chromosomes reorganise into highly compact, rod-shaped forms, thought to consist of consecutive chromatin loops around a central protein scaffold. Condensin complexes are involved in chromatin compaction, but the contribution of other chromatin proteins, DNA sequence and histone modifications is less understood. A large region of fission yeast DNA inserted into a mouse chromosome was previously observed to adopt a mitotic organisation distinct from that of surrounding mouse DNA. Here, we show that a similar distinct structure is common to a large subset of insertion events in both mouse and human cells and is coincident with the presence of high levels of heterochromatic H3 lysine nine trimethylation (H3K9me3). Hi-C and microscopy indicate that the heterochromatinised fission yeast DNA is organised into smaller chromatin loops than flanking euchromatic mouse chromatin. We conclude that heterochromatin alters chromatin loop size, thus contributing to the distinct appearance of heterochromatin on mitotic chromosomes.