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Cost adjusted hierarchical defense strategies enables stratified oxidative stress tolerance

ABSTRACT: Organisms employ diverse adaptive strategies to withstand environmental stresses, yet how bacteria tailor their responses to different magnitudes of the same stressor remains poorly understood. This question is particularly salient for oxidative stress, which varies substantially across physiological niches and exerts distinct selection pressures on colonizing bacterial populations. Here, we used four separate adaptive laboratory evolution (ALE) of Escherichia coli across multiple paraquat concentrations and genetic backgrounds to dissect how cells adapt to varying levels of superoxide stress. Integrating multi-omic analyses with tailored genome-scale metabolic modeling, we identify two fundamentally distinct tolerance strategies based on flux control and cellular resource optimization. Under low superoxide stress, reducing paraquat influx suffices to maintain redox balance. In contrast, higher stress levels activate an energetically demanding program involving enhanced ROS defenses and active efflux. We further show that these flux regulatory responses interface with metabolic repair systems to enable additional fitness gains. Together, our findings reveal how E. coli differentially engages modular stress-response programs depending on stress magnitude, offering generalizable insights into the principles governing dynamic bacterial adaptation.

ORGANISM(S): Escherichia coli str. K-12 substr. MG1655

PROVIDER: GSE316857 | GEO | 2026/03/03

REPOSITORIES: GEO

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Project description:Exposure to Paraquat and RNA interference knockdown of mitochondrial superoxide dismutase (Sod2) are known to result in significant lifespan reduction, locomotor dysfunction, and mitochondrial degeneration in Drosophila melanogaster. Both perturbations increase the flux of superoxide, a progenitor reactive oxygen species, but the molecular underpinnings of the resulting phenotypes are poorly understood. Improved understanding of such processes could lead to advances in the treatment of numerous age-related disorders. Superoxide toxicity can act through protein carbonylation. Analysis of carbonylated proteins is attractive since reactive carbonyl groups are not present in the twenty canonical amino acids and are amenable to labeling and enrichment strategies. Here, carbonylated proteins were labeled with biotin hydrazide and enriched on streptavidin-coated beads. On-bead digestion was used to release carbonylated protein peptides, with relative abundance ratios versus controls obtained using the iTRAQ mass spectrometry-based proteomics approach. While Paraquat exposure and Sod2 knockdown have similar phenotypes, differences in protein carbonylation were anticipated because Paraquat exposure was expected to increase the concentration of superoxide throughout the cell while Sod2 knockdown was only expected to raise the concentration of superoxide in the mitochondrial matrix. Paraquat exposure resulted in widespread increases in carbonylated protein relative abundance: the median Paraquat-exposed to control carbonylated protein relative abundance ratio was 1.53. For Sod2 knockdown, in contrast, the median carbonylated protein relative abundance ratios were 1.13 versus the RNA interference driver control and 1.05 versus the RNA interference transgene control. However, some proteins did show large increases in carbonylated protein relative abundance on Sod2 knockdown, most notably cytochrome c oxidase subunit Vb, possibly providing some indication of the molecular basis of the Sod2-knockdown phenotype.

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Cost adjusted hierarchical defense strategies enables stratified oxidative stress tolerance

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