Metabolomics

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Hierarchical Carbon Metabolism in Iron-Deficient Bacteria Favors Iron-Scavenging Strategy


ABSTRACT:

High-affinity iron (Fe) scavenging compounds, or siderophores, are widely employed by soil bacteria to survive scarcity in bioavailable Fe. Siderophore biosynthesis relies on cellular carbon metabolism, despite reported decrease in both carbon uptake and Fe-containing metabolic proteins in Fe-deficient cells. Given this paradox, the metabolic network required to sustain the Fe-scavenging strategy is poorly understood. Here, through multiple 13C-metabolomics experiments with Fe-replete and Fe-limited cells, we uncover how soil Pseudomonas species reprogram their metabolic pathways to prioritize siderophore biosynthesis. Across the three species investigated (Pseudomonas putida KT2440, Pseudomonas protegens Pf-5, and Pseudomonas putida S12), siderophore secretion is higher during growth on gluconeogenic substrates than during growth on glycolytic substrates. In response to Fe limitation, we capture decreased flux toward the tricarboxylic acid (TCA) cycle during the metabolism of glycolytic substrates but, due to carbon recycling to the TCA cycle via enhanced anaplerosis, the metabolism of gluconeogenic substrates results in an increase in both siderophore secretion (up to threefold) and Fe extraction (up to sixfold) from soil minerals. During simultaneous feeding on the different substrate types, Fe deficiency triggers a hierarchy in substrate utilization, which is facilitated by changes in protein abundances for substrate uptake and initial catabolism. Rerouted metabolism further promotes favorable fluxes in the TCA cycle and the gluconeogenesis-anaplerosis nodes, despite decrease in several proteins in these pathways, to meet carbon and energy demands for siderophore precursors in accordance with increased proteins for siderophore biosynthesis. Hierarchical carbon metabolism thus serves as a critical survival strategy during the metal nutrient deficiency.


Data availability:

The proteomics data have been deposited into the ProteomeXchange Consortium via the PRIDE partner repository with the data set identifier PXD013605.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse phase

SUBMITTER: Caroll Mendonca 

PROVIDER: MTBLS1715 | MetaboLights | 2020-12-05

REPOSITORIES: MetaboLights

Dataset's files

Source:
Action DRS
MTBLS1715 Other
FILES Other
a_MTBLS1715_LC-MS_negative_reverse-phase_metabolite_profiling-1.txt Txt
i_Investigation.txt Txt
m_MTBLS1715_LC-MS_negative_reverse-phase_metabolite_profiling-1_v2_maf.tsv Tabular
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Publications

Hierarchical routing in carbon metabolism favors iron-scavenging strategy in iron-deficient soil <i>Pseudomonas</i> species.

Mendonca Caroll M CM   Yoshitake Sho S   Wei Hua H   Werner Anne A   Sasnow Samantha S SS   Thannhauser Theodore W TW   Aristilde Ludmilla L  

Proceedings of the National Academy of Sciences of the United States of America 20201203 51


High-affinity iron (Fe) scavenging compounds, or siderophores, are widely employed by soil bacteria to survive scarcity in bioavailable Fe. Siderophore biosynthesis relies on cellular carbon metabolism, despite reported decrease in both carbon uptake and Fe-containing metabolic proteins in Fe-deficient cells. Given this paradox, the metabolic network required to sustain the Fe-scavenging strategy is poorly understood. Here, through multiple <sup>13</sup>C-metabolomics experiments with Fe-replete  ...[more]

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