Aspergillus niger Secretes Citrate to Increase Iron Bioavailability

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 under...

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Main Authors: Dorett I. Odoni, Merlijn P. van Gaal, Tom Schonewille, Juan A. Tamayo-Ramos, Vitor A. P. Martins dos Santos, Maria Suarez-Diez, Peter J. Schaap
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-08-01
Series:Frontiers in Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmicb.2017.01424/full
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author Dorett I. Odoni
Merlijn P. van Gaal
Merlijn P. van Gaal
Tom Schonewille
Juan A. Tamayo-Ramos
Vitor A. P. Martins dos Santos
Vitor A. P. Martins dos Santos
Maria Suarez-Diez
Peter J. Schaap
author_facet Dorett I. Odoni
Merlijn P. van Gaal
Merlijn P. van Gaal
Tom Schonewille
Juan A. Tamayo-Ramos
Vitor A. P. Martins dos Santos
Vitor A. P. Martins dos Santos
Maria Suarez-Diez
Peter J. Schaap
author_sort Dorett I. Odoni
collection DOAJ
description 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.
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spelling doaj.art-7551bc34f4a44d1c894e0473751a9e382022-12-22T00:31:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2017-08-01810.3389/fmicb.2017.01424280521Aspergillus niger Secretes Citrate to Increase Iron BioavailabilityDorett I. Odoni0Merlijn P. van Gaal1Merlijn P. van Gaal2Tom Schonewille3Juan A. Tamayo-Ramos4Vitor A. P. Martins dos Santos5Vitor A. P. Martins dos Santos6Maria Suarez-Diez7Peter J. Schaap8Laboratory of System and Synthetic Biology, Wageningen University & ResearchWageningen, NetherlandsLaboratory of System and Synthetic Biology, Wageningen University & ResearchWageningen, NetherlandsLaboratory of Microbiology, Wageningen University & ResearchWageningen, NetherlandsLaboratory of System and Synthetic Biology, Wageningen University & ResearchWageningen, NetherlandsLaboratory of System and Synthetic Biology, Wageningen University & ResearchWageningen, NetherlandsLaboratory of System and Synthetic Biology, Wageningen University & ResearchWageningen, NetherlandsLifeGlimmer GmBHBerlin, GermanyLaboratory of System and Synthetic Biology, Wageningen University & ResearchWageningen, NetherlandsLaboratory of System and Synthetic Biology, Wageningen University & ResearchWageningen, NetherlandsAspergillus 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.http://journal.frontiersin.org/article/10.3389/fmicb.2017.01424/fullAspergillus nigercitrate secretioniron homeostasissiderophoresmetabolic overflow
spellingShingle Dorett I. Odoni
Merlijn P. van Gaal
Merlijn P. van Gaal
Tom Schonewille
Juan A. Tamayo-Ramos
Vitor A. P. Martins dos Santos
Vitor A. P. Martins dos Santos
Maria Suarez-Diez
Peter J. Schaap
Aspergillus niger Secretes Citrate to Increase Iron Bioavailability
Frontiers in Microbiology
Aspergillus niger
citrate secretion
iron homeostasis
siderophores
metabolic overflow
title Aspergillus niger Secretes Citrate to Increase Iron Bioavailability
title_full Aspergillus niger Secretes Citrate to Increase Iron Bioavailability
title_fullStr Aspergillus niger Secretes Citrate to Increase Iron Bioavailability
title_full_unstemmed Aspergillus niger Secretes Citrate to Increase Iron Bioavailability
title_short Aspergillus niger Secretes Citrate to Increase Iron Bioavailability
title_sort aspergillus niger secretes citrate to increase iron bioavailability
topic Aspergillus niger
citrate secretion
iron homeostasis
siderophores
metabolic overflow
url http://journal.frontiersin.org/article/10.3389/fmicb.2017.01424/full
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