Regulation of iron transport related genes by boron in the marine bacterium Marinobacter algicola DG893

Department of Chemistry and Biochemistry, San Diego State University, San Diego, CA 92162-1030, USA. .
Metallomics (Impact Factor: 3.59). 06/2013; 5(8). DOI: 10.1039/c3mt00068k
Source: PubMed


While there has been extensive interest in the use of boron isotope ratios as a surrogate of pH in paleoclimate studies in the context of climate change-related questions, the high (0.4 mM) concentration and the depth-independent (conservative or non-nutrient-like) concentration profile of this element have led to boron being neglected as a potentially biologically relevant element in the modern ocean. Here we report that boron affects the expression of a number of protein and genes in the "algal-associated" Gram-negative marine bacterium Marinobacter algicola DG893. Most intriguingly, a number of these proteins and genes are related to iron uptake. In a recent separate publication we have shown that boron regulates one such iron transport related protein, i.e. the periplasmic iron binding protein FbpA via a direct interaction of the metalloid with this protein. Here we show that a number of other iron uptake related genes are also affected by boron but in the opposite way i.e. they are up-regulated. We propose that the differential effect of boron on FbpA expression relative to other iron transport related genes is a result of an interaction between boron and the global iron regulatory protein Fur.

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Available from: Shady Amin, Jun 26, 2014
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    ABSTRACT: Boron in the ocean is generally considered a non-biological 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 Fe(3+) sequestration by Mb-FbpA at pH 8 (oceanic pH) by acting as a synergistic anion (B(OH)4(1-)). 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 Fe(3+) 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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