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Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut

Author

Listed:
  • Judith Behnsen

    (University of California Irvine
    University of Illinois Chicago)

  • Hui Zhi

    (University of California San Diego)

  • Allegra T. Aron

    (University of California San Diego
    University of California, San Diego)

  • Vivekanandan Subramanian

    (University of Kentucky PharmNMR Center, College of Pharmacy, University of Kentucky)

  • William Santus

    (University of Illinois Chicago)

  • Michael H. Lee

    (University of California San Diego)

  • Romana R. Gerner

    (University of California San Diego)

  • Daniel Petras

    (University of California San Diego
    University of California, San Diego)

  • Janet Z. Liu

    (University of California Irvine)

  • Keith D. Green

    (University of Kentucky)

  • Sarah L. Price

    (University of Louisville School of Medicine)

  • Jose Camacho

    (University of California San Diego)

  • Hannah Hillman

    (University of California San Diego)

  • Joshua Tjokrosurjo

    (University of California Irvine)

  • Nicola P. Montaldo

    (University of California Irvine)

  • Evelyn M. Hoover

    (University of California Irvine)

  • Sean Treacy-Abarca

    (University of California Irvine)

  • Benjamin A. Gilston

    (Vanderbilt University Medical Center)

  • Eric P. Skaar

    (Vanderbilt University Medical Center)

  • Walter J. Chazin

    (Vanderbilt University Medical Center)

  • Sylvie Garneau-Tsodikova

    (University of Kentucky)

  • Matthew B. Lawrenz

    (University of Louisville School of Medicine)

  • Robert D. Perry

    (University of Kentucky)

  • Sean-Paul Nuccio

    (University of California Irvine
    University of California San Diego)

  • Pieter C. Dorrestein

    (University of California San Diego
    University of California, San Diego
    University of California San Diego)

  • Manuela Raffatellu

    (University of California Irvine
    University of California San Diego
    University of California San Diego
    Chiba University-UC San Diego Center for Mucosal Immunology, Allergy, and Vaccines (CU-UCSD cMAV))

Abstract

Zinc is an essential cofactor for bacterial metabolism, and many Enterobacteriaceae express the zinc transporters ZnuABC and ZupT to acquire this metal in the host. However, the probiotic bacterium Escherichia coli Nissle 1917 (or “Nissle”) exhibits appreciable growth in zinc-limited media even when these transporters are deleted. Here, we show that Nissle utilizes the siderophore yersiniabactin as a zincophore, enabling Nissle to grow in zinc-limited media, to tolerate calprotectin-mediated zinc sequestration, and to thrive in the inflamed gut. We also show that yersiniabactin’s affinity for iron or zinc changes in a pH-dependent manner, with increased relative zinc binding as the pH increases. Thus, our results indicate that siderophore metal affinity can be influenced by the local environment and reveal a mechanism of zinc acquisition available to commensal and pathogenic Enterobacteriaceae.

Suggested Citation

  • Judith Behnsen & Hui Zhi & Allegra T. Aron & Vivekanandan Subramanian & William Santus & Michael H. Lee & Romana R. Gerner & Daniel Petras & Janet Z. Liu & Keith D. Green & Sarah L. Price & Jose Camac, 2021. "Siderophore-mediated zinc acquisition enhances enterobacterial colonization of the inflamed gut," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27297-2
    DOI: 10.1038/s41467-021-27297-2
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    References listed on IDEAS

    as
    1. Franziska Faber & Lisa Tran & Mariana X. Byndloss & Christopher A. Lopez & Eric M. Velazquez & Tobias Kerrinnes & Sean-Paul Nuccio & Tamding Wangdi & Oliver Fiehn & Renée M. Tsolis & Andreas J. Bäumle, 2016. "Host-mediated sugar oxidation promotes post-antibiotic pathogen expansion," Nature, Nature, vol. 534(7609), pages 697-699, June.
    2. Martina Sassone-Corsi & Sean-Paul Nuccio & Henry Liu & Dulcemaria Hernandez & Christine T. Vu & Amy A. Takahashi & Robert A. Edwards & Manuela Raffatellu, 2016. "Microcins mediate competition among Enterobacteriaceae in the inflamed gut," Nature, Nature, vol. 540(7632), pages 280-283, December.
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    Cited by:

    1. Ana Carolina Dantas Machado & Stephany Flores Ramos & Julia M. Gauglitz & Anne-Marie Fassler & Daniel Petras & Alexander A. Aksenov & Un Bi Kim & Michael Lazarowicz & Abbey Barnard Giustini & Hamed Ar, 2023. "Portosystemic shunt placement reveals blood signatures for the development of hepatic encephalopathy through mass spectrometry," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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