Iron Modulates the Growth and Activity of Nitrate-Dependent Methanotrophic Bacteria by Reprogramming Carbon Metabolism
Xiangwu Yao, Meng Zhang, Mike S. M. Jetten, Lizhong Zhu, Baolan Hu
Abstract
Iron is indispensable for literally all microorganisms, yet becomes toxic at elevated levels. Protein-based iron storage compartments, such as ferritins, play a key role in maintaining iron homeostasis when the iron level surpasses microbial requirements. However, the energy-intensive nature of iron storage raises questions about how microbes balance this bioprocess between growth and metabolism. Here, using nitrate-dependent methanotrophic bacteria with the simplified metabolic system as a model, we propose a novel metabolic reprogramming pathway regulated by iron storage that controls the balance between growth and activity. Isotopic labeling and meta-omics analyses revealed a striking contrast between bacterial abundance and methane-dependent denitrification activity in “ Ca . M. sinica”. Using microscopy and energy dispersive spectroscopy, we identified iron-rich nanoparticles within cells exposed to 40 μM Fe 2+, alongside increased expression of genes involved in iron metabolism and methane oxidation coupled with denitrification. Additionally, we observed a shift from the energy-demanding Calvin cycle to the more energy-efficient serine pathway for carbon fixation, promoting the synthesis of glycine and succinyl-CoA, which serve as key precursors for iron storage proteins. These metabolic adjustments highlight a strategy for coordinating both substance and energy metabolism in nitrate-dependent methanotrophic bacteria, thereby enhancing their capacity for simultaneous nitrogen and carbon removal. Our findings reveal that iron may act as a metabolic “switch” in microorganisms, offering new insights into the targeted manipulation of microbial metabolism to maximize their beneficial functions in both engineered and natural environments.