Borate as a synergistic anion for marinobacter algicola ferric binding protein, FbpA

A role for boron in iron transport in marine life

Aruna J. Weerasinghe, Shady Amin, Ryan A. Barker, Thaer Othman, Ariel N. Romano, Claire J. Parker Siburt, Jerrell Tisnado, Lisa A. Lambert, Tom Huxford, Carl J. Carrano, Alvin L. Crumbliss

    Research output: Contribution to journalArticle

    Abstract

    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)41-). Fe 3+ sequestration does not occur at pH 6.5 where boric acid (B(OH)3; pKa = 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 pKa 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.

    Original languageEnglish (US)
    Pages (from-to)14504-14507
    Number of pages4
    JournalJournal of the American Chemical Society
    Volume135
    Issue number39
    DOIs
    StatePublished - Oct 2 2013

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    Marinobacter
    Borates
    Boron
    Anions
    Carrier Proteins
    Negative ions
    Iron
    Boric acid
    Oceans and Seas
    Bacteria
    Periplasmic Binding Proteins
    Proteins
    Proteome
    Water

    ASJC Scopus subject areas

    • Catalysis
    • Chemistry(all)
    • Biochemistry
    • Colloid and Surface Chemistry

    Cite this

    Weerasinghe, A. J., Amin, S., Barker, R. A., Othman, T., Romano, A. N., Parker Siburt, C. J., ... Crumbliss, A. L. (2013). Borate as a synergistic anion for marinobacter algicola ferric binding protein, FbpA: A role for boron in iron transport in marine life. Journal of the American Chemical Society, 135(39), 14504-14507. https://doi.org/10.1021/ja406609s

    Borate as a synergistic anion for marinobacter algicola ferric binding protein, FbpA : A role for boron in iron transport in marine life. / Weerasinghe, Aruna J.; Amin, Shady; 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.

    In: Journal of the American Chemical Society, Vol. 135, No. 39, 02.10.2013, p. 14504-14507.

    Research output: Contribution to journalArticle

    Weerasinghe, AJ, Amin, S, Barker, RA, Othman, T, Romano, AN, Parker Siburt, CJ, Tisnado, J, Lambert, LA, Huxford, T, Carrano, CJ & Crumbliss, AL 2013, 'Borate as a synergistic anion for marinobacter algicola ferric binding protein, FbpA: A role for boron in iron transport in marine life', Journal of the American Chemical Society, vol. 135, no. 39, pp. 14504-14507. https://doi.org/10.1021/ja406609s
    Weerasinghe, Aruna J. ; Amin, Shady ; 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. / Borate as a synergistic anion for marinobacter algicola ferric binding protein, FbpA : A role for boron in iron transport in marine life. In: Journal of the American Chemical Society. 2013 ; Vol. 135, No. 39. pp. 14504-14507.
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    AU - Weerasinghe, Aruna J.

    AU - Amin, Shady

    AU - Barker, Ryan A.

    AU - Othman, Thaer

    AU - Romano, Ariel N.

    AU - Parker Siburt, Claire J.

    AU - Tisnado, Jerrell

    AU - Lambert, Lisa A.

    AU - Huxford, Tom

    AU - Carrano, Carl J.

    AU - Crumbliss, Alvin L.

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    N2 - 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)41-). Fe 3+ sequestration does not occur at pH 6.5 where boric acid (B(OH)3; pKa = 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 pKa 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.

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