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Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species

ABSTRACT: Iron (Fe) is an essential micronutrient whose uptake is tightly regulated to balance both deficiency and Fe excess induced oxidative stress. The non-essential heavy metal cadmium (Cd) both induces oxidative stress and an Fe deficiency like response. It is unclear how Cd induces this response, nor how it relates to Fe status sensing. Using next generation sequencing, H2O2 quantification in both wild type and the Fe over-accumulating mutant opt3-2, we explored how Cd interferes with Fe sensing. We found a large overlap of genes consistently responsive to Fe deficiency and Cd in both leaves and roots. Two subnetworks emerged dependent on the high Fe and H2O2 concentration in opt3-2, while opt3-2 chloroplasts showed reduced photosynthetic efficiency during Cd exposure, indicating that they are one source of H2O2. We describe the hierarchical regulation of Fe deficiency responses in the context of the opt3-2 mutant, and demonstrate that the opt3 dependent induction of Fe deficiency responses can be negated, or even reversed, by H2O2 dependent signaling, while the high Fe content of opt3-2 indicates Cd induced iron deficiency is not a function of reduced Fe uptake, but rather the putative leaf Fe sensor is Cd liable.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE128156 | GEO | 2020/07/13

REPOSITORIES: GEO

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Project description: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 <a href='https://www.ebi.ac.uk/pride/archive/projects/PXD013605' rel='noopener noreferrer' target='_blank'>PXD013605</a>.

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Cadmium interference with iron sensing reveals transcriptional programs sensitive and insensitive to reactive oxygen species

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