Borate as a Synergistic Anion for Marinobacter algicola Ferric Binding Protein, FbpA: A Role for Boron in Iron Transport in Marine Life
Boron in the ocean is generally considered a nonbiological element due to its relatively high concentration (0.4 mM) and depth independent concentration profile. Here we report an unexpected role for boron in the iron transport system of the marine bacterium Marinobacter algicola. Proteome analysis...
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Veröffentlicht in: | Journal of the American Chemical Society 2013-10, Vol.135 (39), p.14504-14507 |
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creator | Weerasinghe, Aruna J Amin, Shady A Barker, Ryan A Othman, Thaer Romano, Ariel N Parker Siburt, Claire J Tisnado, Jerrell Lambert, Lisa A Huxford, Tom Carrano, Carl J Crumbliss, Alvin L |
description | Boron in the ocean is generally considered a nonbiological element due to its relatively high concentration (0.4 mM) and depth independent concentration profile. Here we report an unexpected role for boron in the iron transport system of the marine bacterium Marinobacter algicola. Proteome analysis under varying boron concentrations revealed that the periplasmic ferric binding protein (Mb-FbpA) was among the proteins whose expression was most affected, strongly implicating the involvement of boron in iron utilization. Here we show that boron facilitates Fe3+ sequestration by Mb-FbpA at pH 8 (oceanic pH) by acting as a synergistic anion (B(OH)4 1–). Fe3+ sequestration does not occur at pH 6.5 where boric acid (B(OH)3; pK a = 8.55) is the predominant species. Borate anion is also shown to bind to apo-Mb-FbpA with mM affinity at pH 8, consistent with the biological relevance implied from boron’s oceanic concentration (0.4 mM). Borate is among those synergistic anions tested which support the strongest Fe3+ binding to Mb-FbpA, where the range of anion dependent affinity constants is log K′ eff = 21–22. Since the pK a of boric acid (8.55) lies near the pH of ocean water, changes in oceanic pH, as a consequence of fluctuations in atmospheric CO2, may perturb iron uptake in many marine heterotrophic bacteria due to a decrease in oceanic borate anion concentration. |
doi_str_mv | 10.1021/ja406609s |
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Here we report an unexpected role for boron in the iron transport system of the marine bacterium Marinobacter algicola. Proteome analysis under varying boron concentrations revealed that the periplasmic ferric binding protein (Mb-FbpA) was among the proteins whose expression was most affected, strongly implicating the involvement of boron in iron utilization. Here we show that boron facilitates Fe3+ sequestration by Mb-FbpA at pH 8 (oceanic pH) by acting as a synergistic anion (B(OH)4 1–). Fe3+ sequestration does not occur at pH 6.5 where boric acid (B(OH)3; pK a = 8.55) is the predominant species. Borate anion is also shown to bind to apo-Mb-FbpA with mM affinity at pH 8, consistent with the biological relevance implied from boron’s oceanic concentration (0.4 mM). Borate is among those synergistic anions tested which support the strongest Fe3+ binding to Mb-FbpA, where the range of anion dependent affinity constants is log K′ eff = 21–22. Since the pK a of boric acid (8.55) lies near the pH of ocean water, changes in oceanic pH, as a consequence of fluctuations in atmospheric CO2, may perturb iron uptake in many marine heterotrophic bacteria due to a decrease in oceanic borate anion concentration.</description><identifier>ISSN: 0002-7863</identifier><identifier>EISSN: 1520-5126</identifier><identifier>DOI: 10.1021/ja406609s</identifier><identifier>PMID: 24028339</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Anions - metabolism ; Bacterial Proteins - metabolism ; Borates - metabolism ; Boron - metabolism ; Iron - metabolism ; Iron-Binding Proteins - metabolism ; Marinobacter - metabolism ; Models, Molecular</subject><ispartof>Journal of the American Chemical Society, 2013-10, Vol.135 (39), p.14504-14507</ispartof><rights>Copyright © 2013 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a315t-ae4aa609c88992b8898457e08c0994eff8e668a73fa0333c98a36cd615fd88c03</citedby><cites>FETCH-LOGICAL-a315t-ae4aa609c88992b8898457e08c0994eff8e668a73fa0333c98a36cd615fd88c03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/ja406609s$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/ja406609s$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,780,784,2765,27076,27924,27925,56738,56788</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24028339$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Weerasinghe, Aruna J</creatorcontrib><creatorcontrib>Amin, Shady A</creatorcontrib><creatorcontrib>Barker, Ryan A</creatorcontrib><creatorcontrib>Othman, Thaer</creatorcontrib><creatorcontrib>Romano, Ariel N</creatorcontrib><creatorcontrib>Parker Siburt, Claire J</creatorcontrib><creatorcontrib>Tisnado, Jerrell</creatorcontrib><creatorcontrib>Lambert, Lisa A</creatorcontrib><creatorcontrib>Huxford, Tom</creatorcontrib><creatorcontrib>Carrano, Carl J</creatorcontrib><creatorcontrib>Crumbliss, Alvin L</creatorcontrib><title>Borate as a Synergistic Anion for Marinobacter algicola Ferric Binding Protein, FbpA: A Role for Boron in Iron Transport in Marine Life</title><title>Journal of the American Chemical Society</title><addtitle>J. Am. Chem. Soc</addtitle><description>Boron in the ocean is generally considered a nonbiological element due to its relatively high concentration (0.4 mM) and depth independent concentration profile. Here we report an unexpected role for boron in the iron transport system of the marine bacterium Marinobacter algicola. Proteome analysis under varying boron concentrations revealed that the periplasmic ferric binding protein (Mb-FbpA) was among the proteins whose expression was most affected, strongly implicating the involvement of boron in iron utilization. Here we show that boron facilitates Fe3+ sequestration by Mb-FbpA at pH 8 (oceanic pH) by acting as a synergistic anion (B(OH)4 1–). Fe3+ sequestration does not occur at pH 6.5 where boric acid (B(OH)3; pK a = 8.55) is the predominant species. Borate anion is also shown to bind to apo-Mb-FbpA with mM affinity at pH 8, consistent with the biological relevance implied from boron’s oceanic concentration (0.4 mM). Borate is among those synergistic anions tested which support the strongest Fe3+ binding to Mb-FbpA, where the range of anion dependent affinity constants is log K′ eff = 21–22. Since the pK a of boric acid (8.55) lies near the pH of ocean water, changes in oceanic pH, as a consequence of fluctuations in atmospheric CO2, may perturb iron uptake in many marine heterotrophic bacteria due to a decrease in oceanic borate anion concentration.</description><subject>Anions - metabolism</subject><subject>Bacterial Proteins - metabolism</subject><subject>Borates - metabolism</subject><subject>Boron - metabolism</subject><subject>Iron - metabolism</subject><subject>Iron-Binding Proteins - metabolism</subject><subject>Marinobacter - metabolism</subject><subject>Models, Molecular</subject><issn>0002-7863</issn><issn>1520-5126</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNptkMFOAjEQhhujEUQPvoDpxUQTV9ttd-l6QyJKgtEonjdDmSUlS4vtcuAJfG2LICcvnXTyzTeZn5Bzzm45S_ndHCTLc1aEA9LmWcqSjKf5IWkzxtKkq3LRIichzONXpoofk1YqWaqEKNrk-8F5aJBCoEA_1hb9zITGaNqzxllaOU9fwBvrJqAb9BTqmdGuBjpA7yP2YOzU2Bl9865BY2_oYLLs3dMefXc1_o7HBVFkLB1u6tiDDUvnm03n14x0ZCo8JUcV1AHPdrVDPgeP4_5zMnp9GvZ7owQEz5oEUALES7VSRZFO4qtk1kWmNCsKiVWlMM8VdEUFTAihCwUi19OcZ9VURUh0yNXWu_Tua4WhKRcmaKxrsOhWoeRSCqGyLpMRvd6i2rsQPFbl0psF-HXJWbnJvdznHtmLnXY1WeB0T_4FHYHLLQA6lHO38jZe-Y_oBwJfiL4</recordid><startdate>20131002</startdate><enddate>20131002</enddate><creator>Weerasinghe, Aruna J</creator><creator>Amin, Shady A</creator><creator>Barker, Ryan A</creator><creator>Othman, Thaer</creator><creator>Romano, Ariel N</creator><creator>Parker Siburt, Claire J</creator><creator>Tisnado, Jerrell</creator><creator>Lambert, Lisa A</creator><creator>Huxford, Tom</creator><creator>Carrano, Carl J</creator><creator>Crumbliss, Alvin L</creator><general>American Chemical Society</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>7X8</scope></search><sort><creationdate>20131002</creationdate><title>Borate as a Synergistic Anion for Marinobacter algicola Ferric Binding Protein, FbpA: A Role for Boron in Iron Transport in Marine Life</title><author>Weerasinghe, Aruna J ; Amin, Shady A ; Barker, Ryan A ; Othman, Thaer ; Romano, Ariel N ; Parker Siburt, Claire J ; Tisnado, Jerrell ; Lambert, Lisa A ; Huxford, Tom ; Carrano, Carl J ; Crumbliss, Alvin L</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a315t-ae4aa609c88992b8898457e08c0994eff8e668a73fa0333c98a36cd615fd88c03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Anions - metabolism</topic><topic>Bacterial Proteins - metabolism</topic><topic>Borates - metabolism</topic><topic>Boron - metabolism</topic><topic>Iron - metabolism</topic><topic>Iron-Binding Proteins - metabolism</topic><topic>Marinobacter - metabolism</topic><topic>Models, Molecular</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Weerasinghe, Aruna J</creatorcontrib><creatorcontrib>Amin, Shady A</creatorcontrib><creatorcontrib>Barker, Ryan A</creatorcontrib><creatorcontrib>Othman, Thaer</creatorcontrib><creatorcontrib>Romano, Ariel N</creatorcontrib><creatorcontrib>Parker Siburt, Claire J</creatorcontrib><creatorcontrib>Tisnado, Jerrell</creatorcontrib><creatorcontrib>Lambert, Lisa A</creatorcontrib><creatorcontrib>Huxford, Tom</creatorcontrib><creatorcontrib>Carrano, Carl J</creatorcontrib><creatorcontrib>Crumbliss, Alvin L</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Journal of the American Chemical Society</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Weerasinghe, Aruna J</au><au>Amin, Shady A</au><au>Barker, Ryan A</au><au>Othman, Thaer</au><au>Romano, Ariel N</au><au>Parker Siburt, Claire J</au><au>Tisnado, Jerrell</au><au>Lambert, Lisa A</au><au>Huxford, Tom</au><au>Carrano, Carl J</au><au>Crumbliss, Alvin L</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Borate as a Synergistic Anion for Marinobacter algicola Ferric Binding Protein, FbpA: A Role for Boron in Iron Transport in Marine Life</atitle><jtitle>Journal of the American Chemical Society</jtitle><addtitle>J. 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Borate anion is also shown to bind to apo-Mb-FbpA with mM affinity at pH 8, consistent with the biological relevance implied from boron’s oceanic concentration (0.4 mM). Borate is among those synergistic anions tested which support the strongest Fe3+ binding to Mb-FbpA, where the range of anion dependent affinity constants is log K′ eff = 21–22. Since the pK a of boric acid (8.55) lies near the pH of ocean water, changes in oceanic pH, as a consequence of fluctuations in atmospheric CO2, may perturb iron uptake in many marine heterotrophic bacteria due to a decrease in oceanic borate anion concentration.</abstract><cop>United States</cop><pub>American Chemical Society</pub><pmid>24028339</pmid><doi>10.1021/ja406609s</doi><tpages>4</tpages></addata></record> |
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subjects | Anions - metabolism Bacterial Proteins - metabolism Borates - metabolism Boron - metabolism Iron - metabolism Iron-Binding Proteins - metabolism Marinobacter - metabolism Models, Molecular |
title | Borate as a Synergistic Anion for Marinobacter algicola Ferric Binding Protein, FbpA: A Role for Boron in Iron Transport in Marine Life |
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