Siderophore-mediated iron acquisition by Klebsiella pneumoniae
Microbes synthesize and secrete siderophores, that bind and solubilize precipitated or otherwise unavailable iron in their microenvironments. Gram (-) bacterial TonB-dependent outer membrane receptors capture the resulting ferric siderophores to begin the uptake process. From their similarity to the...
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creator | Kumar, Ashish Chakravorty, Somnath Yang, Taihao Russo, Thomas A Newton, Salete M Klebba, Phillip E |
description | Microbes synthesize and secrete siderophores, that bind and solubilize precipitated or otherwise unavailable iron in their microenvironments. Gram (-) bacterial TonB-dependent outer membrane receptors capture the resulting ferric siderophores to begin the uptake process. From their similarity to
the structural gene for the
ferric enterobactin (FeEnt) receptor, we identified four homologous genes in the human and animal ESKAPE pathogen
(strain Kp52.145). One locus encodes IroN (locus
on plasmid pII), and three other loci encode other FepA orthologs/paralogs (chromosomal loci
and
). Based on the crystal structure of
FepA (1FEP), we modeled the tertiary structures of the
FepA homologs and genetically engineered individual Cys substitutions in their predicted surface loops. We subjected bacteria expressing the Cys mutant proteins to modification with extrinsic fluorescein maleimide (FM) and used the resulting fluorescently labeled cells to spectroscopically monitor the binding and transport of catecholate ferric siderophores by the four different receptors. The FM-modified FepA homologs were nanosensors that defined the ferric catecholate uptake pathways in pathogenic strains of
. In Kp52.145, loci
and
encoded receptors that primarily recognized and transported FeEnt; locus
produced a receptor that principally bound and transported FeEnt and glucosylated FeEnt (FeGEnt); locus 2380 encoded a protein that bound ferric catecholate compounds but did not detectably transport them. The sensors also characterized the uptake of iron complexes, including FeGEnt, by the hypervirulent, hypermucoviscous
strain hvKp1.
Both commensal and pathogenic bacteria produce small organic chelators, called siderophores, that avidly bind iron and increase its bioavailability.
variably produces four siderophores that antagonize host iron sequestration: enterobactin, glucosylated enterobactin (also termed salmochelin), aerobactin, and yersiniabactin, which promote colonization of different host tissues. Abundant evidence links bacterial iron acquisition to virulence and infectious diseases. The data we report explain the recognition and transport of ferric catecholates and other siderophores, which are crucial to iron acquisition by
. |
doi_str_mv | 10.1128/jb.00024-24 |
format | Article |
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the structural gene for the
ferric enterobactin (FeEnt) receptor, we identified four homologous genes in the human and animal ESKAPE pathogen
(strain Kp52.145). One locus encodes IroN (locus
on plasmid pII), and three other loci encode other FepA orthologs/paralogs (chromosomal loci
and
). Based on the crystal structure of
FepA (1FEP), we modeled the tertiary structures of the
FepA homologs and genetically engineered individual Cys substitutions in their predicted surface loops. We subjected bacteria expressing the Cys mutant proteins to modification with extrinsic fluorescein maleimide (FM) and used the resulting fluorescently labeled cells to spectroscopically monitor the binding and transport of catecholate ferric siderophores by the four different receptors. The FM-modified FepA homologs were nanosensors that defined the ferric catecholate uptake pathways in pathogenic strains of
. In Kp52.145, loci
and
encoded receptors that primarily recognized and transported FeEnt; locus
produced a receptor that principally bound and transported FeEnt and glucosylated FeEnt (FeGEnt); locus 2380 encoded a protein that bound ferric catecholate compounds but did not detectably transport them. The sensors also characterized the uptake of iron complexes, including FeGEnt, by the hypervirulent, hypermucoviscous
strain hvKp1.
Both commensal and pathogenic bacteria produce small organic chelators, called siderophores, that avidly bind iron and increase its bioavailability.
variably produces four siderophores that antagonize host iron sequestration: enterobactin, glucosylated enterobactin (also termed salmochelin), aerobactin, and yersiniabactin, which promote colonization of different host tissues. Abundant evidence links bacterial iron acquisition to virulence and infectious diseases. The data we report explain the recognition and transport of ferric catecholates and other siderophores, which are crucial to iron acquisition by
.</description><identifier>ISSN: 0021-9193</identifier><identifier>ISSN: 1098-5530</identifier><identifier>EISSN: 1098-5530</identifier><identifier>DOI: 10.1128/jb.00024-24</identifier><identifier>PMID: 38591913</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>Bacteria ; Cell surface receptors ; Crystal structure ; E coli ; Enterobactin ; Genetic engineering ; Iron ; Klebsiella ; Klebsiella pneumoniae ; Microbial Pathogenesis ; Microenvironments ; Nanosensors ; Pathogens ; Proteins ; Receptors ; Research Article ; Siderophores ; Spectrum analysis</subject><ispartof>Journal of bacteriology, 2024-05, Vol.206 (5), p.e0002424</ispartof><rights>Copyright © 2024 American Society for Microbiology.</rights><rights>Copyright American Society for Microbiology May 2024</rights><rights>Copyright © 2024 American Society for Microbiology. 2024 American Society for Microbiology.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a364t-a2ae85c2ffe34f0ab3e10b728c2868b7b5089e79321d6a499a8452651c48c9743</cites><orcidid>0000-0003-4566-7442 ; 0000-0002-6979-3083</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11112993/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11112993/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38591913$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Comstock, Laurie E.</contributor><creatorcontrib>Kumar, Ashish</creatorcontrib><creatorcontrib>Chakravorty, Somnath</creatorcontrib><creatorcontrib>Yang, Taihao</creatorcontrib><creatorcontrib>Russo, Thomas A</creatorcontrib><creatorcontrib>Newton, Salete M</creatorcontrib><creatorcontrib>Klebba, Phillip E</creatorcontrib><title>Siderophore-mediated iron acquisition by Klebsiella pneumoniae</title><title>Journal of bacteriology</title><addtitle>J Bacteriol</addtitle><addtitle>J Bacteriol</addtitle><description>Microbes synthesize and secrete siderophores, that bind and solubilize precipitated or otherwise unavailable iron in their microenvironments. Gram (-) bacterial TonB-dependent outer membrane receptors capture the resulting ferric siderophores to begin the uptake process. From their similarity to
the structural gene for the
ferric enterobactin (FeEnt) receptor, we identified four homologous genes in the human and animal ESKAPE pathogen
(strain Kp52.145). One locus encodes IroN (locus
on plasmid pII), and three other loci encode other FepA orthologs/paralogs (chromosomal loci
and
). Based on the crystal structure of
FepA (1FEP), we modeled the tertiary structures of the
FepA homologs and genetically engineered individual Cys substitutions in their predicted surface loops. We subjected bacteria expressing the Cys mutant proteins to modification with extrinsic fluorescein maleimide (FM) and used the resulting fluorescently labeled cells to spectroscopically monitor the binding and transport of catecholate ferric siderophores by the four different receptors. The FM-modified FepA homologs were nanosensors that defined the ferric catecholate uptake pathways in pathogenic strains of
. In Kp52.145, loci
and
encoded receptors that primarily recognized and transported FeEnt; locus
produced a receptor that principally bound and transported FeEnt and glucosylated FeEnt (FeGEnt); locus 2380 encoded a protein that bound ferric catecholate compounds but did not detectably transport them. The sensors also characterized the uptake of iron complexes, including FeGEnt, by the hypervirulent, hypermucoviscous
strain hvKp1.
Both commensal and pathogenic bacteria produce small organic chelators, called siderophores, that avidly bind iron and increase its bioavailability.
variably produces four siderophores that antagonize host iron sequestration: enterobactin, glucosylated enterobactin (also termed salmochelin), aerobactin, and yersiniabactin, which promote colonization of different host tissues. Abundant evidence links bacterial iron acquisition to virulence and infectious diseases. The data we report explain the recognition and transport of ferric catecholates and other siderophores, which are crucial to iron acquisition by
.</description><subject>Bacteria</subject><subject>Cell surface receptors</subject><subject>Crystal structure</subject><subject>E coli</subject><subject>Enterobactin</subject><subject>Genetic engineering</subject><subject>Iron</subject><subject>Klebsiella</subject><subject>Klebsiella pneumoniae</subject><subject>Microbial Pathogenesis</subject><subject>Microenvironments</subject><subject>Nanosensors</subject><subject>Pathogens</subject><subject>Proteins</subject><subject>Receptors</subject><subject>Research Article</subject><subject>Siderophores</subject><subject>Spectrum analysis</subject><issn>0021-9193</issn><issn>1098-5530</issn><issn>1098-5530</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNptkUlLBDEUhIMoOi4n7zLgRZDW7J1cFBE3HPCgnkPS81ozdHfGpFvw3xu3ccFcEl4-6lVRCG0TfEAIVYczd4AxprygfAmNCNaqEILhZTTKU1JootkaWk9phjHhXNBVtMaUyGPCRujo1k8hhvljiFC0MPW2h-nYx9CNbfU0-OR7n9_uZXzdgEsemsaO5x0Mbei8hU20UtsmwdbnvYHuz8_uTi-Lyc3F1enJpLBM8r6w1IISFa1rYLzG1jEg2JVUVVRJ5UonsNJQakbJVFqutVXZqBSk4qrSJWcb6PhDdz647LKCro-2MfPoWxtfTLDe_P7p_KN5CM-G5EO1Zllh71MhhqcBUm9an6q3OB2EIRmGmcAll5JmdPcPOgtD7HK-TEkutSipzNT-B1XFkFKEeuGGYPNWjJk5816Mofx7vU0t_db7H935mXUh-1UaewXoFpTX</recordid><startdate>20240523</startdate><enddate>20240523</enddate><creator>Kumar, Ashish</creator><creator>Chakravorty, Somnath</creator><creator>Yang, Taihao</creator><creator>Russo, Thomas A</creator><creator>Newton, Salete M</creator><creator>Klebba, Phillip E</creator><general>American Society for Microbiology</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QL</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4566-7442</orcidid><orcidid>https://orcid.org/0000-0002-6979-3083</orcidid></search><sort><creationdate>20240523</creationdate><title>Siderophore-mediated iron acquisition by Klebsiella pneumoniae</title><author>Kumar, Ashish ; Chakravorty, Somnath ; Yang, Taihao ; Russo, Thomas A ; Newton, Salete M ; Klebba, Phillip E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a364t-a2ae85c2ffe34f0ab3e10b728c2868b7b5089e79321d6a499a8452651c48c9743</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Bacteria</topic><topic>Cell surface receptors</topic><topic>Crystal structure</topic><topic>E coli</topic><topic>Enterobactin</topic><topic>Genetic engineering</topic><topic>Iron</topic><topic>Klebsiella</topic><topic>Klebsiella pneumoniae</topic><topic>Microbial Pathogenesis</topic><topic>Microenvironments</topic><topic>Nanosensors</topic><topic>Pathogens</topic><topic>Proteins</topic><topic>Receptors</topic><topic>Research Article</topic><topic>Siderophores</topic><topic>Spectrum analysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kumar, Ashish</creatorcontrib><creatorcontrib>Chakravorty, Somnath</creatorcontrib><creatorcontrib>Yang, Taihao</creatorcontrib><creatorcontrib>Russo, Thomas A</creatorcontrib><creatorcontrib>Newton, Salete M</creatorcontrib><creatorcontrib>Klebba, Phillip E</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of bacteriology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kumar, Ashish</au><au>Chakravorty, Somnath</au><au>Yang, Taihao</au><au>Russo, Thomas A</au><au>Newton, Salete M</au><au>Klebba, Phillip E</au><au>Comstock, Laurie E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Siderophore-mediated iron acquisition by Klebsiella pneumoniae</atitle><jtitle>Journal of bacteriology</jtitle><stitle>J Bacteriol</stitle><addtitle>J Bacteriol</addtitle><date>2024-05-23</date><risdate>2024</risdate><volume>206</volume><issue>5</issue><spage>e0002424</spage><pages>e0002424-</pages><issn>0021-9193</issn><issn>1098-5530</issn><eissn>1098-5530</eissn><abstract>Microbes synthesize and secrete siderophores, that bind and solubilize precipitated or otherwise unavailable iron in their microenvironments. Gram (-) bacterial TonB-dependent outer membrane receptors capture the resulting ferric siderophores to begin the uptake process. From their similarity to
the structural gene for the
ferric enterobactin (FeEnt) receptor, we identified four homologous genes in the human and animal ESKAPE pathogen
(strain Kp52.145). One locus encodes IroN (locus
on plasmid pII), and three other loci encode other FepA orthologs/paralogs (chromosomal loci
and
). Based on the crystal structure of
FepA (1FEP), we modeled the tertiary structures of the
FepA homologs and genetically engineered individual Cys substitutions in their predicted surface loops. We subjected bacteria expressing the Cys mutant proteins to modification with extrinsic fluorescein maleimide (FM) and used the resulting fluorescently labeled cells to spectroscopically monitor the binding and transport of catecholate ferric siderophores by the four different receptors. The FM-modified FepA homologs were nanosensors that defined the ferric catecholate uptake pathways in pathogenic strains of
. In Kp52.145, loci
and
encoded receptors that primarily recognized and transported FeEnt; locus
produced a receptor that principally bound and transported FeEnt and glucosylated FeEnt (FeGEnt); locus 2380 encoded a protein that bound ferric catecholate compounds but did not detectably transport them. The sensors also characterized the uptake of iron complexes, including FeGEnt, by the hypervirulent, hypermucoviscous
strain hvKp1.
Both commensal and pathogenic bacteria produce small organic chelators, called siderophores, that avidly bind iron and increase its bioavailability.
variably produces four siderophores that antagonize host iron sequestration: enterobactin, glucosylated enterobactin (also termed salmochelin), aerobactin, and yersiniabactin, which promote colonization of different host tissues. Abundant evidence links bacterial iron acquisition to virulence and infectious diseases. The data we report explain the recognition and transport of ferric catecholates and other siderophores, which are crucial to iron acquisition by
.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>38591913</pmid><doi>10.1128/jb.00024-24</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-4566-7442</orcidid><orcidid>https://orcid.org/0000-0002-6979-3083</orcidid></addata></record> |
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subjects | Bacteria Cell surface receptors Crystal structure E coli Enterobactin Genetic engineering Iron Klebsiella Klebsiella pneumoniae Microbial Pathogenesis Microenvironments Nanosensors Pathogens Proteins Receptors Research Article Siderophores Spectrum analysis |
title | Siderophore-mediated iron acquisition by Klebsiella pneumoniae |
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