Hierarchical routing in carbon metabolism favors iron-scavenging strategy in iron-deficient soil
| Autor: | Caroll M, Mendonca, Sho, Yoshitake, Hua, Wei, Anne, Werner, Samantha S, Sasnow, Theodore W, Thannhauser, Ludmilla, Aristilde |
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| Rok vydání: | 2020 |
| Předmět: |
Carbon Isotopes
iron limitation siderophore Pseudomonas putida Iron Citric Acid Cycle Gluconeogenesis Succinic Acid Siderophores Biological Sciences Biochemistry metabolomics Carbon Enzymes Pseudomonas Physical Sciences bacteria Oligopeptides Metabolic Networks and Pathways Soil Microbiology Environmental Sciences |
| Zdroj: | Proceedings of the National Academy of Sciences of the United States of America |
| ISSN: | 1091-6490 |
| Popis: | Significance Siderophore secretion confers competitive advantage to pathogenic and beneficial bacteria in various nutritional environments, including human infections and rhizosphere microbiome. The siderophore biosynthesis must be sustained during a compromised carbon metabolism in Fe-deficient cells. Here we demonstrate that Fe-deficient Pseudomonas species overcome this paradox by coupling selectivity in carbon utilization with a hierarchy in metabolic pathways to favor carbon and energy fluxes for siderophore biosynthesis. A reprogrammed metabolism is predicted from genomics-based data obtained with several marine and soil bacterial systems in response to Fe deficiency, but metabolomics evidence is lacking. The present study offers an important roadmap for investigating the underlying metabolic connections between Fe or other metal nutrient availability and carbon utilization. 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. |
| Databáze: | OpenAIRE |
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