Host-induced spermidine production in motile Pseudomonas aeruginosa triggers phagocytic uptake

Abstract

Exploring the complexity of host-pathogen communication is vital to understand why<br /> microbes persist within a host, while others are cleared. Here, we employed a Dual-sequencing approach to unravel conversational turn-taking of dynamic host-pathogen communications. We demonstrate that upon hitting a host cell, motile Pseudomonas aeruginosa induce a specific gene expression program. This results in the expression of spermidine on the surface, which specifically activates the PIP3-pathway to induce phagocytic uptake into primary or immortalized murine cells. Non-motile bacteria are more immunogenic due to a lower expression of arnT upon host cell contact, but do not produce spermidine and are phagocytosed less. We demonstrate that not only the presence of pathogen inherent molecular patterns induces immune responses, but that bacterial motility is linked to a host-cell induced expression of additional immune modulators. Our results emphasize on the value of integrating microbiological and immunological findings to unravel complex and dynamic host-pathogen interactions.

Data availability

Raw files and reads per gene of the RNA sequencing approaches have been deposited in the NCBI Gene Expression Omnibus (GEO) under the accession number GSE141757.

The following data sets were generated

Article and author information

Author details

  1. Sebastian Felgner

    Molecular Bacteriology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0030-2490
  2. Matthias Preusse

    Molecular Bacteriology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Ulrike Beutling

    Chemical Biology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Stephanie Stahnke

    Cell biology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Vinay Pawar

    Molecular Bacteriology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Manfred Rohde

    Central Facility for Microscopy, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Mark Brönstrup

    Department of Chemical Biology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8971-7045
  8. Theresia Stradal

    Cell biology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Susanne Häussler

    Molecular Bacteriology, Helmholtz Centre for Infection Research, Braunschweig, Germany
    For correspondence
    susanne.haeussler@helmholtz-hzi.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6141-9102

Funding

ERC Consolidator Grant COMBAT (724290)

  • Susanne Häussler

DFG, Germany's Excellence Strategy - EXC 2155 RESIST (390874280)

  • Susanne Häussler

SPP (1879)

  • Susanne Häussler

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

Ethics

Animal experimentation: All animal experiments were performed according to guidelines of the German Law for Animal Protection and with permission of the local ethics committee and the local authority LAVES (Niedersächsisches Landesamt für Verbraucherschutz und Lebensmittelsicherheit). C57BL/6 mice derived from our own breeding.

Reviewing Editor

  1. Sophie Helaine, Harvard Medical School, United States

Publication history

  1. Received: February 4, 2020
  2. Accepted: September 15, 2020
  3. Accepted Manuscript published: September 22, 2020 (version 1)
  4. Version of Record published: October 6, 2020 (version 2)

Copyright

© 2020, Felgner 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.

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  1. Sebastian Felgner
  2. Matthias Preusse
  3. Ulrike Beutling
  4. Stephanie Stahnke
  5. Vinay Pawar
  6. Manfred Rohde
  7. Mark Brönstrup
  8. Theresia Stradal
  9. Susanne Häussler
(2020)
Host-induced spermidine production in motile Pseudomonas aeruginosa triggers phagocytic uptake
eLife 9:e55744.
https://doi.org/10.7554/eLife.55744

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