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Bacterial iron acquisition mediated by outer membrane translocation and cleavage of a host protein
Iron is an essential micronutrient for most bacteria and is obtained from iron-chelating siderophores or directly from iron-containing host proteins. For Gram-negative bacteria, classical iron transport systems consist of an outer membrane receptor, a periplasmic binding protein, and an inner membra...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 2018-06, Vol.115 (26), p.6840-6845 |
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description | Iron is an essential micronutrient for most bacteria and is obtained from iron-chelating siderophores or directly from iron-containing host proteins. For Gram-negative bacteria, classical iron transport systems consist of an outer membrane receptor, a periplasmic binding protein, and an inner membrane ABC transporter, which work in concert to deliver iron from the cell surface to the cytoplasm. We recently showed that Pectobacterium spp. are able to acquire iron from ferredoxin, a small and stable 2Fe-2S iron sulfur cluster containing protein and identified the ferredoxin receptor, FusA, a TonB-dependent receptor that binds ferredoxin on the cell surface. The genetic context of fusA suggests an atypical iron acquisition system, lacking a periplasmic binding protein, although the mechanism through which iron is extracted from the captured ferredoxin has remained unknown. Here we show that FusC, an M16 family protease, displays a highly targeted proteolytic activity against plant ferredoxin, and that growth enhancement of Pectobacterium due to iron acquisition from ferredoxin is FusC-dependent. The periplasmic location of FusC indicates a mechanism in which ferredoxin is imported into the periplasm via FusA before cleavage by FusC, as confirmed by the uptake and accumulation of ferredoxin in the periplasm in a strain lacking fusC. The existence of homologous uptake systems in a range of pathogenic bacteria suggests that protein uptake for nutrient acquisition may be widespread in bacteria and shows that, similar to their endosymbiotic descendants mitochondria and chloroplasts, bacteria produce dedicated protein import systems. |
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For Gram-negative bacteria, classical iron transport systems consist of an outer membrane receptor, a periplasmic binding protein, and an inner membrane ABC transporter, which work in concert to deliver iron from the cell surface to the cytoplasm. We recently showed that Pectobacterium spp. are able to acquire iron from ferredoxin, a small and stable 2Fe-2S iron sulfur cluster containing protein and identified the ferredoxin receptor, FusA, a TonB-dependent receptor that binds ferredoxin on the cell surface. The genetic context of fusA suggests an atypical iron acquisition system, lacking a periplasmic binding protein, although the mechanism through which iron is extracted from the captured ferredoxin has remained unknown. Here we show that FusC, an M16 family protease, displays a highly targeted proteolytic activity against plant ferredoxin, and that growth enhancement of Pectobacterium due to iron acquisition from ferredoxin is FusC-dependent. The periplasmic location of FusC indicates a mechanism in which ferredoxin is imported into the periplasm via FusA before cleavage by FusC, as confirmed by the uptake and accumulation of ferredoxin in the periplasm in a strain lacking fusC. The existence of homologous uptake systems in a range of pathogenic bacteria suggests that protein uptake for nutrient acquisition may be widespread in bacteria and shows that, similar to their endosymbiotic descendants mitochondria and chloroplasts, bacteria produce dedicated protein import systems.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1800672115</identifier><identifier>PMID: 29891657</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>ABC transporter ; Bacteria ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biological Sciences ; Cell Membrane - genetics ; Cell Membrane - metabolism ; Cell surface ; Chelation ; Chloroplasts ; Cleavage ; Cytoplasm ; Ferredoxin ; Gram-negative bacteria ; Homology ; Iron ; Iron - metabolism ; Membrane proteins ; Membrane Proteins - genetics ; Membrane Proteins - metabolism ; Membranes ; Mitochondria ; Nutrient uptake ; Pectobacterium ; Pectobacterium - genetics ; Pectobacterium - metabolism ; Peptide Elongation Factor G - genetics ; Peptide Elongation Factor G - metabolism ; Periplasm ; Periplasm - genetics ; Periplasm - metabolism ; Proteases ; Protein transport ; Proteins ; Proteolysis ; Siderophores ; Sulfur ; Translocation</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2018-06, Vol.115 (26), p.6840-6845</ispartof><rights>Volumes 1–89 and 106–114, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright © 2018 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Jun 26, 2018</rights><rights>Copyright © 2018 the Author(s). Published by PNAS. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-5c9626b30d8ba3960a3c3ed2e0fcf02885d8dab3992a268307c906c23dbf322e3</citedby><cites>FETCH-LOGICAL-c509t-5c9626b30d8ba3960a3c3ed2e0fcf02885d8dab3992a268307c906c23dbf322e3</cites><orcidid>0000-0002-4206-2942</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26510824$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26510824$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29891657$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mosbahi, Khedidja</creatorcontrib><creatorcontrib>Wojnowska, Marta</creatorcontrib><creatorcontrib>Albalat, Amaya</creatorcontrib><creatorcontrib>Walker, Daniel</creatorcontrib><title>Bacterial iron acquisition mediated by outer membrane translocation and cleavage of a host protein</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Iron is an essential micronutrient for most bacteria and is obtained from iron-chelating siderophores or directly from iron-containing host proteins. For Gram-negative bacteria, classical iron transport systems consist of an outer membrane receptor, a periplasmic binding protein, and an inner membrane ABC transporter, which work in concert to deliver iron from the cell surface to the cytoplasm. We recently showed that Pectobacterium spp. are able to acquire iron from ferredoxin, a small and stable 2Fe-2S iron sulfur cluster containing protein and identified the ferredoxin receptor, FusA, a TonB-dependent receptor that binds ferredoxin on the cell surface. The genetic context of fusA suggests an atypical iron acquisition system, lacking a periplasmic binding protein, although the mechanism through which iron is extracted from the captured ferredoxin has remained unknown. Here we show that FusC, an M16 family protease, displays a highly targeted proteolytic activity against plant ferredoxin, and that growth enhancement of Pectobacterium due to iron acquisition from ferredoxin is FusC-dependent. The periplasmic location of FusC indicates a mechanism in which ferredoxin is imported into the periplasm via FusA before cleavage by FusC, as confirmed by the uptake and accumulation of ferredoxin in the periplasm in a strain lacking fusC. The existence of homologous uptake systems in a range of pathogenic bacteria suggests that protein uptake for nutrient acquisition may be widespread in bacteria and shows that, similar to their endosymbiotic descendants mitochondria and chloroplasts, bacteria produce dedicated protein import systems.</description><subject>ABC transporter</subject><subject>Bacteria</subject><subject>Bacterial Proteins - genetics</subject><subject>Bacterial Proteins - metabolism</subject><subject>Biological Sciences</subject><subject>Cell Membrane - genetics</subject><subject>Cell Membrane - metabolism</subject><subject>Cell surface</subject><subject>Chelation</subject><subject>Chloroplasts</subject><subject>Cleavage</subject><subject>Cytoplasm</subject><subject>Ferredoxin</subject><subject>Gram-negative bacteria</subject><subject>Homology</subject><subject>Iron</subject><subject>Iron - metabolism</subject><subject>Membrane proteins</subject><subject>Membrane Proteins - genetics</subject><subject>Membrane Proteins - metabolism</subject><subject>Membranes</subject><subject>Mitochondria</subject><subject>Nutrient uptake</subject><subject>Pectobacterium</subject><subject>Pectobacterium - genetics</subject><subject>Pectobacterium - metabolism</subject><subject>Peptide Elongation Factor G - genetics</subject><subject>Peptide Elongation Factor G - metabolism</subject><subject>Periplasm</subject><subject>Periplasm - genetics</subject><subject>Periplasm - metabolism</subject><subject>Proteases</subject><subject>Protein transport</subject><subject>Proteins</subject><subject>Proteolysis</subject><subject>Siderophores</subject><subject>Sulfur</subject><subject>Translocation</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNpdkUFvFSEUhYnR2Nfq2pWGxE03015gYGBjUhtbTZq4adfkDsO0vMwbXoFp0n8vz1dbdQPk3o-Tc3II-cDghEEnTrcz5hOmAVTHGZOvyIqBYY1qDbwmKwDeNbrl7QE5zHkNAEZqeEsOuNGGKdmtSP8VXfEp4ERDijNFd7-EHEqo740fAhY_0P6RxqVSdbLpE86elnrmKTr8DeI8UDd5fMBbT-NIkd7FXOg2xeLD_I68GXHK_v3TfURuLr5dn39vrn5e_jg_u2qcBFMa6Yziqhcw6B6FUYDCCT9wD6MbgWstBz1gL4zhyJUW0DkDynEx9KPg3Isj8mWvu136at35ubqc7DaFDaZHGzHYfzdzuLO38cEqaDl0pgocPwmkeL_4XOwmZOenqSaOS7YcZGtk17Y79PN_6Douaa7xLGcAWjMDolKne8qlmHPy47MZBnbXn931Z1_6qz8-_Z3hmf9TWAU-7oF1LjG97JVkoHkrfgGtzqH9</recordid><startdate>20180626</startdate><enddate>20180626</enddate><creator>Mosbahi, Khedidja</creator><creator>Wojnowska, Marta</creator><creator>Albalat, Amaya</creator><creator>Walker, Daniel</creator><general>National Academy of Sciences</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</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/0000-0002-4206-2942</orcidid></search><sort><creationdate>20180626</creationdate><title>Bacterial iron acquisition mediated by outer membrane translocation and cleavage of a host protein</title><author>Mosbahi, Khedidja ; 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For Gram-negative bacteria, classical iron transport systems consist of an outer membrane receptor, a periplasmic binding protein, and an inner membrane ABC transporter, which work in concert to deliver iron from the cell surface to the cytoplasm. We recently showed that Pectobacterium spp. are able to acquire iron from ferredoxin, a small and stable 2Fe-2S iron sulfur cluster containing protein and identified the ferredoxin receptor, FusA, a TonB-dependent receptor that binds ferredoxin on the cell surface. The genetic context of fusA suggests an atypical iron acquisition system, lacking a periplasmic binding protein, although the mechanism through which iron is extracted from the captured ferredoxin has remained unknown. Here we show that FusC, an M16 family protease, displays a highly targeted proteolytic activity against plant ferredoxin, and that growth enhancement of Pectobacterium due to iron acquisition from ferredoxin is FusC-dependent. The periplasmic location of FusC indicates a mechanism in which ferredoxin is imported into the periplasm via FusA before cleavage by FusC, as confirmed by the uptake and accumulation of ferredoxin in the periplasm in a strain lacking fusC. The existence of homologous uptake systems in a range of pathogenic bacteria suggests that protein uptake for nutrient acquisition may be widespread in bacteria and shows that, similar to their endosymbiotic descendants mitochondria and chloroplasts, bacteria produce dedicated protein import systems.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>29891657</pmid><doi>10.1073/pnas.1800672115</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0002-4206-2942</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | ABC transporter Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Biological Sciences Cell Membrane - genetics Cell Membrane - metabolism Cell surface Chelation Chloroplasts Cleavage Cytoplasm Ferredoxin Gram-negative bacteria Homology Iron Iron - metabolism Membrane proteins Membrane Proteins - genetics Membrane Proteins - metabolism Membranes Mitochondria Nutrient uptake Pectobacterium Pectobacterium - genetics Pectobacterium - metabolism Peptide Elongation Factor G - genetics Peptide Elongation Factor G - metabolism Periplasm Periplasm - genetics Periplasm - metabolism Proteases Protein transport Proteins Proteolysis Siderophores Sulfur Translocation |
title | Bacterial iron acquisition mediated by outer membrane translocation and cleavage of a host protein |
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