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Enterobacteria secrete an inhibitor of Pseudomonas virulence during clinical bacteriuria
Shannon I. Ohlemacher, … , Barbara W. Trautner, Jeffrey P. Henderson
Shannon I. Ohlemacher, … , Barbara W. Trautner, Jeffrey P. Henderson
Published September 25, 2017
Citation Information: J Clin Invest. 2017;127(11):4018-4030. https://doi.org/10.1172/JCI92464.
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Research Article Infectious disease

Enterobacteria secrete an inhibitor of Pseudomonas virulence during clinical bacteriuria

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Abstract

Escherichia coli and other Enterobacteriaceae are among the most common pathogens of the human urinary tract. Among the genetic gains of function associated with urinary E. coli isolates is the Yersinia high pathogenicity island (HPI), which directs the biosynthesis of yersiniabactin (Ybt), a virulence-associated metallophore. Using a metabolomics approach, we found that E. coli and other Enterobacteriaceae expressing the Yersinia HPI also secrete escherichelin, a second metallophore whose chemical structure matches a known synthetic inhibitor of the virulence-associated pyochelin siderophore system in Pseudomonas aeruginosa. We detected escherichelin during clinical E. coli urinary tract infection (UTI) and experimental human colonization with a commensal, potentially probiotic E. coli bacteriuria strain. Escherichelin production by colonizing enterobacteria may help human hosts resist opportunistic infections by Pseudomonas and other pyochelin-expressing bacteria. This siderophore-based mechanism of microbial antagonism may be one of many elements contributing to the protective effects of the human microbiome. Future UTI-preventive probiotic strains may benefit by retaining the escherichelin biosynthetic capacity of the Yersinia HPI while eliminating the Ybt biosynthetic capacity.

Authors

Shannon I. Ohlemacher, Daryl E. Giblin, D. André d’Avignon, Ann E. Stapleton, Barbara W. Trautner, Jeffrey P. Henderson

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Figure 1

Metabolomic analysis reveals escherichelin as an additional product of Ybt-producing E. coli.

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Metabolomic analysis reveals escherichelin as an additional product of Y...
(A) Two-group PCA-DA of LC-MS data demonstrate consistent variance in the secreted metabolomes of the Ybt producers, WT UTI89 and UTI89ΔybtS chemically complemented with salicylic acid (SA), and the nonproducer UTI89ΔybtS. Each point indicates the average of 3 technical replicates. Five biological replicates were analyzed from each experimental group. (B) The PCA-DA loadings plot, where each point is a molecular feature identified in the LC-MS analysis, reveals a molecular feature with m/z 307 (escherichelin) that best distinguishes Ybt producers from nonproducers. (C) LC-MS/MS chromatograms of escherichelin (left) and apo-Ybt (right) from culture supernatants of Enterobacteriaceae isolates grown in iron-restricted medium. All of the strains that produced Ybt also produced escherichelin.

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ISSN: 0021-9738 (print), 1558-8238 (online)

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