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

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 Camacho, Hannah Hillman, Joshua Tjokrosurjo, Nicola P. Montaldo, Evelyn M. Hoover, Sean Treacy-Abarca, Benjamin A. Gilston, Eric P. Skaar, Walter J. Chazin, Sylvie Garneau-Tsodikova, Matthew B. Lawrenz, Robert D. Perry, Sean-Paul Nuccio, Pieter C. Dorrestein and Manuela Raffatellu ()
Additional contact information
Judith Behnsen: University of California Irvine
Hui Zhi: University of California San Diego
Allegra T. Aron: 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
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
Pieter C. Dorrestein: University of California San Diego
Manuela Raffatellu: University of California Irvine

Nature Communications, 2021, vol. 12, issue 1, 1-15

Abstract: 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.

Date: 2021
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DOI: 10.1038/s41467-021-27297-2

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