Aspergillus niger secretes citrate to increase iron bioavailability

Research output: Contribution to journalArticleAcademicpeer-review

4 Citations (Scopus)

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.
LanguageEnglish
Article number1424
JournalFrontiers in Microbiology
Volume8
Issue numberAUG
DOIs
Publication statusPublished - 2017

Fingerprint

Aspergillus niger
Citric Acid
Biological Availability
Iron
Acids
Culture Media
Siderophores
Oxalates
Up-Regulation
Nitrogen
Enzymes
Growth

Keywords

  • Aspergillus niger
  • Citrate secretion
  • Iron homeostasis
  • Metabolic overflow
  • Siderophores

Cite this

@article{4524b4fc27394e63a7b3e0b79630dd78,
title = "Aspergillus niger secretes citrate to increase iron bioavailability",
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.",
keywords = "Aspergillus niger, Citrate secretion, Iron homeostasis, Metabolic overflow, Siderophores",
author = "Odoni, {Dorett I.} and {van Gaal}, {Merlijn P.} and Tom Schonewille and Tamayo-Ramos, {Juan A.} and {Martins dos Santos}, {Vitor A.P.} and Maria Suarez-Diez and Schaap, {Peter J.}",
year = "2017",
doi = "10.3389/fmicb.2017.01424",
language = "English",
volume = "8",
journal = "Frontiers in Microbiology",
issn = "1664-302X",
publisher = "Frontiers",
number = "AUG",

}

Aspergillus niger secretes citrate to increase iron bioavailability. / Odoni, Dorett I.; van Gaal, Merlijn P.; Schonewille, Tom; Tamayo-Ramos, Juan A.; Martins dos Santos, Vitor A.P.; Suarez-Diez, Maria; Schaap, Peter J.

In: Frontiers in Microbiology, Vol. 8, No. AUG, 1424, 2017.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Aspergillus niger secretes citrate to increase iron bioavailability

AU - Odoni, Dorett I.

AU - van Gaal, Merlijn P.

AU - Schonewille, Tom

AU - Tamayo-Ramos, Juan A.

AU - Martins dos Santos, Vitor A.P.

AU - Suarez-Diez, Maria

AU - Schaap, Peter J.

PY - 2017

Y1 - 2017

N2 - 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.

AB - 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.

KW - Aspergillus niger

KW - Citrate secretion

KW - Iron homeostasis

KW - Metabolic overflow

KW - Siderophores

U2 - 10.3389/fmicb.2017.01424

DO - 10.3389/fmicb.2017.01424

M3 - Article

VL - 8

JO - Frontiers in Microbiology

T2 - Frontiers in Microbiology

JF - Frontiers in Microbiology

SN - 1664-302X

IS - AUG

M1 - 1424

ER -