Abstract
Aspergillus niger has an innate ability to secrete various organic acids, including citrate. The conditions required for A. niger citrate overproduction are well described, but the physiological reasons underlying extracellular citrate accumulation are not yet fully understood. One of the less understood culture conditions is the requirement of growth-limiting iron concentrations. While this has been attributed to iron-dependent citrate metabolizing enzymes, this straightforward relationship does not always hold true. Here, we show that an increase in citrate secretion under iron limited conditions is a physiological response consistent with a role of citrate as A. niger iron siderophore. We found that A. niger citrate secretion increases with decreasing amounts of iron added to the culture medium and, in contrast to previous findings, this response is independent of the nitrogen source. Differential transcriptomics analyses of the two A. niger mutants NW305 (gluconate non-producer) and NW186 (gluconate and oxalate non-producer) revealed up-regulation of the citrate biosynthesis gene citA under iron limited conditions compared to iron replete conditions. In addition, we show that A. niger can utilize Fe(III) citrate as iron source. Finally, we discuss our findings in the general context of the pH-dependency of A. niger organic acid production, offering an explanation, besides competition, for why A. niger organic acid production is a sequential process influenced by the external pH of the culture medium.
Highlights
The filamentous fungus Aspergillus niger has an innate ability to secrete organic acids in high quantities, and is essential as a biotechnological citrate producer (Schuster et al, 2002)
We investigated the effect of iron limitation on the A. niger transcriptome, and found changes associated to biomass, iron siderophore, and citrate and oxalate biosynthesis genes
There are two possible interpretations for the results presented in Figure 2: (i) A. niger citrate production is a result of metabolic overflow triggered by carbon excess relative to low iron availability, or (ii) A. niger citrate production is a strategy to increase bioavailability of iron
Summary
The filamentous fungus Aspergillus niger has an innate ability to secrete organic acids in high quantities, and is essential as a biotechnological citrate producer (Schuster et al, 2002). On glucose as carbon source, wild type A. niger secretes gluconate and oxalate as well as citrate. To inhibit by-production of gluconate and oxalate, A. niger citrate production requires pH ≤ 2.5 and the absence of manganese (Mn2+) ions, thereby enforcing overproduction of citrate instead (Currie, 1917; Kubicek and Röhr, 1977; Ruijter et al, 1999). Further production conditions that have been reported to influence external citrate accumulation are, amongst others, the choice and concentrations of the carbon and nitrogen sources, and the concentrations of trace elements in the culture medium (Karaffa and Kubicek, 2003). Suggested to be the basis of industrial A. niger citrate production (Neilands, 1981), the physiological reason underlying the particular requirement of suboptimal iron concentrations to prompt increased A. niger citrate secretion is not yet fully understood. Ferrous (Fe(II)) iron is oxidized to ferric
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