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Title: Tailoring a Global Iron Regulon to a Uropathogen

Abstract

Pathogenicity islands and plasmids bear genes for pathogenesis of various Escherichia coli pathotypes. Although there is a basic understanding of the contribution of these virulence factors to disease, less is known about variation in regulatory networks in determining disease phenotypes. Here, we dissected a regulatory network directed by the conserved iron homeostasis regulator, ferric uptake regulator (Fur), in uropathogenic E. coli (UPEC) strain CFT073. Comparing anaerobic genome-scale Fur DNA binding with Fur-dependent transcript expression and protein levels of the uropathogen to that of commensal E. coli K-12 strain MG1655 showed that the Fur regulon of the core genome is conserved but also includes genes within the pathogenicity/genetic islands. Unexpectedly, regulons indicative of amino acid limitation and the general stress response were also indirectly activated in the uropathogen fur mutant, suggesting that induction of the Fur regulon increases amino acid demand. Using RpoS levels as a proxy, addition of amino acids mitigated the stress. In addition, iron chelation increased RpoS to the same levels as in the fur mutant. The increased amino acid demand of the fur mutant or iron chelated cells was exacerbated by aerobic conditions, which could be partly explained by the O2-dependent synthesis of the siderophore aerobactin, encodedmore » by an operon within a pathogenicity island. Taken together, these data suggest that in the iron-poor environment of the urinary tract, amino acid availability could play a role in the proliferation of this uropathogen, particularly if there is sufficient O2 to produce aerobactin. IMPORTANCE Host iron restriction is a common mechanism for limiting the growth of pathogens. We compared the regulatory network controlled by Fur in uropathogenic E. coli (UPEC) to that of nonpathogenic E. coli K-12 to uncover strategies that pathogenic bacteria use to overcome iron limitation. Although iron homeostasis functions were regulated by Fur in the uropathogen as expected, a surprising finding was the activation of the stringent and general stress responses in the uropathogen fur mutant, which was rescued by amino acid addition. This coordinated global response could be important in controlling growth and survival under nutrient-limiting conditions and during transitions from the nutrient-rich environment of the lower gastrointestinal (GI) tract to the more restrictive environment of the urinary tract. The coupling of the response of iron limitation to increased demand for amino acids could be a critical attribute that sets UPEC apart from other E. coli pathotypes.« less

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1]
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  1. Univ. of Wisconsin, Madison, WI (United States)
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1680026
Grant/Contract Number:  
SC0018409
Resource Type:
Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Name: mBio (Online); Journal Volume: 11; Journal Issue: 2; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Fur; RyhB; iron regulation; CFT073; UPEC; ppGpp; metabolic adaptation; Sigma S

Citation Formats

Banerjee, Rajdeep, Weisenhorn, Erin, Schwartz, Kevin J., Myers, Kevin S., Glasner, Jeremy D., Perna, Nicole T., Coon, Joshua J., Welch, Rodney A., and Kiley, Patricia J. Tailoring a Global Iron Regulon to a Uropathogen. United States: N. p., 2020. Web. doi:10.1128/mbio.00351-20.
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Banerjee, Rajdeep, Weisenhorn, Erin, Schwartz, Kevin J., Myers, Kevin S., Glasner, Jeremy D., Perna, Nicole T., Coon, Joshua J., Welch, Rodney A., & Kiley, Patricia J. Tailoring a Global Iron Regulon to a Uropathogen. United States. https://doi.org/10.1128/mbio.00351-20
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Banerjee, Rajdeep, Weisenhorn, Erin, Schwartz, Kevin J., Myers, Kevin S., Glasner, Jeremy D., Perna, Nicole T., Coon, Joshua J., Welch, Rodney A., and Kiley, Patricia J. Tue . "Tailoring a Global Iron Regulon to a Uropathogen". United States. https://doi.org/10.1128/mbio.00351-20. https://www.osti.gov/servlets/purl/1680026.
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@article{osti_1680026,
title = {Tailoring a Global Iron Regulon to a Uropathogen},
author = {Banerjee, Rajdeep and Weisenhorn, Erin and Schwartz, Kevin J. and Myers, Kevin S. and Glasner, Jeremy D. and Perna, Nicole T. and Coon, Joshua J. and Welch, Rodney A. and Kiley, Patricia J.},
abstractNote = {Pathogenicity islands and plasmids bear genes for pathogenesis of various Escherichia coli pathotypes. Although there is a basic understanding of the contribution of these virulence factors to disease, less is known about variation in regulatory networks in determining disease phenotypes. Here, we dissected a regulatory network directed by the conserved iron homeostasis regulator, ferric uptake regulator (Fur), in uropathogenic E. coli (UPEC) strain CFT073. Comparing anaerobic genome-scale Fur DNA binding with Fur-dependent transcript expression and protein levels of the uropathogen to that of commensal E. coli K-12 strain MG1655 showed that the Fur regulon of the core genome is conserved but also includes genes within the pathogenicity/genetic islands. Unexpectedly, regulons indicative of amino acid limitation and the general stress response were also indirectly activated in the uropathogen fur mutant, suggesting that induction of the Fur regulon increases amino acid demand. Using RpoS levels as a proxy, addition of amino acids mitigated the stress. In addition, iron chelation increased RpoS to the same levels as in the fur mutant. The increased amino acid demand of the fur mutant or iron chelated cells was exacerbated by aerobic conditions, which could be partly explained by the O2-dependent synthesis of the siderophore aerobactin, encoded by an operon within a pathogenicity island. Taken together, these data suggest that in the iron-poor environment of the urinary tract, amino acid availability could play a role in the proliferation of this uropathogen, particularly if there is sufficient O2 to produce aerobactin. IMPORTANCE Host iron restriction is a common mechanism for limiting the growth of pathogens. We compared the regulatory network controlled by Fur in uropathogenic E. coli (UPEC) to that of nonpathogenic E. coli K-12 to uncover strategies that pathogenic bacteria use to overcome iron limitation. Although iron homeostasis functions were regulated by Fur in the uropathogen as expected, a surprising finding was the activation of the stringent and general stress responses in the uropathogen fur mutant, which was rescued by amino acid addition. This coordinated global response could be important in controlling growth and survival under nutrient-limiting conditions and during transitions from the nutrient-rich environment of the lower gastrointestinal (GI) tract to the more restrictive environment of the urinary tract. The coupling of the response of iron limitation to increased demand for amino acids could be a critical attribute that sets UPEC apart from other E. coli pathotypes.},
doi = {10.1128/mbio.00351-20},
journal = {mBio (Online)},
number = 2,
volume = 11,
place = {United States},
year = {2020},
month = {3}
}
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https://doi.org/10.1128/mbio.00351-20
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Figures / Tables:

FIG 1 FIG 1: Genome-scale differences in Fur-dependent expression between UPEC strain CFT073 and commensal E. coli strain MG1655. E. coli strains were grown under anaerobic, iron-sufficient conditions. (a and b) Venn diagrams comparing the number of differentially expressed RNAs or proteins (> 2-fold change in expression and P < 0.05) inmore » the Δfur mutant strains relative to parent strains CFT073 and MG1655 (32). The region of overlap indicates RNAs (a) or proteins (b) that are regulated by Fur in both CFT073 (pink circle) and MG1655 (gray circle). Fur-regulated CFT073 genes that have no orthologs in strain MG1655 are indicated by the smaller dark pink circle. (c) Volcano plot comparing Fur-regulated proteins from strains CFT073 and MG1655. The x axis indicates the log2 fold change in protein levels in the Δfur mutant/wild-type (wt) strain of CFT073 (red) and MG1655 (gray). The y axis represents –log10 P values for individual proteins. Examples of CFT073-specific proteins (blue font) and orthologous proteins (black font) are indicated. (d) Comparison of genome-wide Fur binding from strains CFT073 and MG1655. The x axis indicates the genomic position of Fur ChIP-seq peaks from CFT073 (version NC_004431.1; top panel) or MG1655 (version U00096.2; bottom panel). The y axis indicates the normalized sequencing read count (in arbitrary units [a.u.]). Enrichment of Fur DNA binding is indicated by the height of the lines in each track. Examples of ChIP-seq peaks upstream of CFT073-specific genes are indicated in blue font, and conservation of ChIP-seq peaks upstream of orthologous genes (black font) is indicated by the orange dashed lines. A complete list of CFT073 ChIP-seq peaks is shown in Table S3 in the supplemental material.« less
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