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A role for PchHI as the ABC transporter in iron acquisition by the siderophore pyochelin in Pseudomonas aeruginosa
Summary Iron is an essential nutrient for bacterial growth but poorly bioavailable. Bacteria scavenge ferric iron by synthesizing and secreting siderophores, small compounds with a high affinity for iron. Pyochelin (PCH) is one of the two siderophores produced by the opportunistic pathogen Pseudomon...
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Published in: | Environmental microbiology 2022-02, Vol.24 (2), p.866-877 |
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creator | Roche, Béatrice Garcia‐Rivera, Mariel A. Normant, Vincent Kuhn, Lauriane Hammann, Philippe Brönstrup, Mark Mislin, Gaëtan L. A. Schalk, Isabelle J. |
description | Summary
Iron is an essential nutrient for bacterial growth but poorly bioavailable. Bacteria scavenge ferric iron by synthesizing and secreting siderophores, small compounds with a high affinity for iron. Pyochelin (PCH) is one of the two siderophores produced by the opportunistic pathogen Pseudomonas aeruginosa. After capturing a ferric iron molecule, PCH‐Fe is imported back into bacteria first by the outer membrane transporter FptA and then by the inner membrane permease FptX. Here, using molecular biology, 55Fe uptake assays, and LC–MS/MS quantification, we first find a role for PchHI as the heterodimeric ABC transporter involved in the siderophore‐free iron uptake into the bacterial cytoplasm. We also provide the first evidence that PCH is able to reach the bacterial periplasm and cytoplasm when both FptA and FptX are expressed. Finally, we detected an interaction between PchH and FptX, linking the ABC transporter PchHI with the inner permease FptX in the PCH‐Fe uptake pathway. These results pave the way for a better understanding of the PCH siderophore pathway, giving future directions to tackle P. aeruginosa infections. |
doi_str_mv | 10.1111/1462-2920.15811 |
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Iron is an essential nutrient for bacterial growth but poorly bioavailable. Bacteria scavenge ferric iron by synthesizing and secreting siderophores, small compounds with a high affinity for iron. Pyochelin (PCH) is one of the two siderophores produced by the opportunistic pathogen Pseudomonas aeruginosa. After capturing a ferric iron molecule, PCH‐Fe is imported back into bacteria first by the outer membrane transporter FptA and then by the inner membrane permease FptX. Here, using molecular biology, 55Fe uptake assays, and LC–MS/MS quantification, we first find a role for PchHI as the heterodimeric ABC transporter involved in the siderophore‐free iron uptake into the bacterial cytoplasm. We also provide the first evidence that PCH is able to reach the bacterial periplasm and cytoplasm when both FptA and FptX are expressed. Finally, we detected an interaction between PchH and FptX, linking the ABC transporter PchHI with the inner permease FptX in the PCH‐Fe uptake pathway. These results pave the way for a better understanding of the PCH siderophore pathway, giving future directions to tackle P. aeruginosa infections.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.15811</identifier><identifier>PMID: 34664350</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>ABC transporter ; ABC transporters ; ATP-Binding Cassette Transporters - genetics ; ATP-Binding Cassette Transporters - metabolism ; Bacteria ; Bacterial Outer Membrane Proteins - genetics ; Bacterial Outer Membrane Proteins - metabolism ; Bacteriology ; Bioavailability ; Biochemistry ; Biochemistry, Molecular Biology ; Biology ; Chromatography, Liquid ; Cytoplasm ; Iron ; Iron - metabolism ; Life Sciences ; Membranes ; Microbiology and Parasitology ; Molecular biology ; Opportunist infection ; Pathogens ; Periplasm ; Permease ; Phenols ; Pseudomonas aeruginosa ; Pseudomonas aeruginosa - genetics ; Pseudomonas aeruginosa - metabolism ; Receptors, Cell Surface - metabolism ; Siderophores ; Siderophores - metabolism ; Tandem Mass Spectrometry ; Thiazoles ; Uptake</subject><ispartof>Environmental microbiology, 2022-02, Vol.24 (2), p.866-877</ispartof><rights>2021 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2022 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4461-61b473cf2dedc8e98b297db80965f09419a4afe31320d184e14942610ab8d54e3</citedby><cites>FETCH-LOGICAL-c4461-61b473cf2dedc8e98b297db80965f09419a4afe31320d184e14942610ab8d54e3</cites><orcidid>0000-0002-9007-7014 ; 0000-0002-8351-1679 ; 0000-0002-2637-1024 ; 0000-0002-6883-9203 ; 0000-0002-2639-1498</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34664350$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03404109$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Roche, Béatrice</creatorcontrib><creatorcontrib>Garcia‐Rivera, Mariel A.</creatorcontrib><creatorcontrib>Normant, Vincent</creatorcontrib><creatorcontrib>Kuhn, Lauriane</creatorcontrib><creatorcontrib>Hammann, Philippe</creatorcontrib><creatorcontrib>Brönstrup, Mark</creatorcontrib><creatorcontrib>Mislin, Gaëtan L. A.</creatorcontrib><creatorcontrib>Schalk, Isabelle J.</creatorcontrib><title>A role for PchHI as the ABC transporter in iron acquisition by the siderophore pyochelin in Pseudomonas aeruginosa</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
Iron is an essential nutrient for bacterial growth but poorly bioavailable. Bacteria scavenge ferric iron by synthesizing and secreting siderophores, small compounds with a high affinity for iron. Pyochelin (PCH) is one of the two siderophores produced by the opportunistic pathogen Pseudomonas aeruginosa. After capturing a ferric iron molecule, PCH‐Fe is imported back into bacteria first by the outer membrane transporter FptA and then by the inner membrane permease FptX. Here, using molecular biology, 55Fe uptake assays, and LC–MS/MS quantification, we first find a role for PchHI as the heterodimeric ABC transporter involved in the siderophore‐free iron uptake into the bacterial cytoplasm. We also provide the first evidence that PCH is able to reach the bacterial periplasm and cytoplasm when both FptA and FptX are expressed. Finally, we detected an interaction between PchH and FptX, linking the ABC transporter PchHI with the inner permease FptX in the PCH‐Fe uptake pathway. These results pave the way for a better understanding of the PCH siderophore pathway, giving future directions to tackle P. aeruginosa infections.</description><subject>ABC transporter</subject><subject>ABC transporters</subject><subject>ATP-Binding Cassette Transporters - genetics</subject><subject>ATP-Binding Cassette Transporters - metabolism</subject><subject>Bacteria</subject><subject>Bacterial Outer Membrane Proteins - genetics</subject><subject>Bacterial Outer Membrane Proteins - metabolism</subject><subject>Bacteriology</subject><subject>Bioavailability</subject><subject>Biochemistry</subject><subject>Biochemistry, Molecular Biology</subject><subject>Biology</subject><subject>Chromatography, Liquid</subject><subject>Cytoplasm</subject><subject>Iron</subject><subject>Iron - metabolism</subject><subject>Life Sciences</subject><subject>Membranes</subject><subject>Microbiology and Parasitology</subject><subject>Molecular biology</subject><subject>Opportunist infection</subject><subject>Pathogens</subject><subject>Periplasm</subject><subject>Permease</subject><subject>Phenols</subject><subject>Pseudomonas aeruginosa</subject><subject>Pseudomonas aeruginosa - genetics</subject><subject>Pseudomonas aeruginosa - metabolism</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>Siderophores</subject><subject>Siderophores - metabolism</subject><subject>Tandem Mass Spectrometry</subject><subject>Thiazoles</subject><subject>Uptake</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNqF0b1P3DAYBnALgQqFzmyVJZZ2uOLXdj48HifaO-kQDDBbTvKmMcrFwU5A99_XIfSGLvXiD_38yNZDyCWwHxDHNciUL7jicZvkAEfk7HByfFgDPyWfQ3hmDDKRsU_kVMg0lSJhZ8QvqXct0tp5-lA26w01gQ4N0uXNig7edKF3fkBPbUetdx015ctogx1sXBf7dxpshd71jfNI-70rG2wn3dGHgGPldq6LmQb9-Nt2LpgLclKbNuCXj_mcPP28fVytF9v7X5vVcrsopUxhkUIhM1HWvMKqzFHlBVdZVeRMpUnNlARlpKlRgOCsglwiSCV5CswUeZVIFOfk-5zbmFb33u6M32tnrF4vt3o6Y0IyCUy9QrTfZtt79zJiGPTOhhLb1nToxqB5kgspM8gnevUPfXaj7-JPNE8Fz4SKLqrrWZXeheCxPrwAmJ6q01M5eipKv1cXb3z9yB2LHVYH_7erCJIZvNkW9__L07d3mzn4D4KloNg</recordid><startdate>202202</startdate><enddate>202202</enddate><creator>Roche, Béatrice</creator><creator>Garcia‐Rivera, Mariel A.</creator><creator>Normant, Vincent</creator><creator>Kuhn, Lauriane</creator><creator>Hammann, Philippe</creator><creator>Brönstrup, Mark</creator><creator>Mislin, Gaëtan L. 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A.</au><au>Schalk, Isabelle J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A role for PchHI as the ABC transporter in iron acquisition by the siderophore pyochelin in Pseudomonas aeruginosa</atitle><jtitle>Environmental microbiology</jtitle><addtitle>Environ Microbiol</addtitle><date>2022-02</date><risdate>2022</risdate><volume>24</volume><issue>2</issue><spage>866</spage><epage>877</epage><pages>866-877</pages><issn>1462-2912</issn><eissn>1462-2920</eissn><abstract>Summary
Iron is an essential nutrient for bacterial growth but poorly bioavailable. Bacteria scavenge ferric iron by synthesizing and secreting siderophores, small compounds with a high affinity for iron. Pyochelin (PCH) is one of the two siderophores produced by the opportunistic pathogen Pseudomonas aeruginosa. After capturing a ferric iron molecule, PCH‐Fe is imported back into bacteria first by the outer membrane transporter FptA and then by the inner membrane permease FptX. Here, using molecular biology, 55Fe uptake assays, and LC–MS/MS quantification, we first find a role for PchHI as the heterodimeric ABC transporter involved in the siderophore‐free iron uptake into the bacterial cytoplasm. We also provide the first evidence that PCH is able to reach the bacterial periplasm and cytoplasm when both FptA and FptX are expressed. Finally, we detected an interaction between PchH and FptX, linking the ABC transporter PchHI with the inner permease FptX in the PCH‐Fe uptake pathway. These results pave the way for a better understanding of the PCH siderophore pathway, giving future directions to tackle P. aeruginosa infections.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>34664350</pmid><doi>10.1111/1462-2920.15811</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-9007-7014</orcidid><orcidid>https://orcid.org/0000-0002-8351-1679</orcidid><orcidid>https://orcid.org/0000-0002-2637-1024</orcidid><orcidid>https://orcid.org/0000-0002-6883-9203</orcidid><orcidid>https://orcid.org/0000-0002-2639-1498</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | ABC transporter ABC transporters ATP-Binding Cassette Transporters - genetics ATP-Binding Cassette Transporters - metabolism Bacteria Bacterial Outer Membrane Proteins - genetics Bacterial Outer Membrane Proteins - metabolism Bacteriology Bioavailability Biochemistry Biochemistry, Molecular Biology Biology Chromatography, Liquid Cytoplasm Iron Iron - metabolism Life Sciences Membranes Microbiology and Parasitology Molecular biology Opportunist infection Pathogens Periplasm Permease Phenols Pseudomonas aeruginosa Pseudomonas aeruginosa - genetics Pseudomonas aeruginosa - metabolism Receptors, Cell Surface - metabolism Siderophores Siderophores - metabolism Tandem Mass Spectrometry Thiazoles Uptake |
title | A role for PchHI as the ABC transporter in iron acquisition by the siderophore pyochelin in Pseudomonas aeruginosa |
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