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

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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