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Combining multiple stressors unexpectedly blocks bacterial migration and growth

ABSTRACT: In nature, organisms experience combinations of stressors. However, laboratory studies use batch cultures, which simplify reality and focus on population-level responses to individual stressors. In recent years, bacterial stress responses have been examined with single-cell resolution using microfluidics. Here, we use a microfluidic approach to simultaneously provide a physical stressor (shear flow) and a chemical stressor (H2O2) to the human pathogen Pseudomonas aeruginosa. By treating cells with levels of flow and H2O2 that commonly co-occur in human host tissues, we discover that previous reports significantly overestimate the H2O2 levels required to block bacterial growth. Specifically, we establish that flow increases H2O2 effectiveness 50-fold, explaining why previous studies lacking flow required much higher concentrations. Using natural H2O2 levels, we identify the core H2O2 regulon, characterize OxyR-mediated dynamic regulation, and demonstrate that multiple H2O2 scavenging systems have redundant roles. By examining single-cell behavior, we serendipitously discover that the combined effects of H2O2 and flow block pilus-driven surface migration. Thus, our results counter previous studies and reveal that natural levels of H2O2 and flow synergize to restrict bacterial motility and survival. By studying two stressors at once, our research highlights the limitations of oversimplifying nature and demonstrates that physical and chemical stress can combine to yield unpredictable effects.

ORGANISM(S): Pseudomonas aeruginosa PA14

PROVIDER: GSE277811 | GEO | 2024/09/30

REPOSITORIES: GEO

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Project description:The health and resilience of species in natural environments are increasingly challenged by complex anthropogenic stressor combinations including climate change, habitat encroachment, and chemical contamination. To better understand impacts of these stressors, we examined the individual- and combined-stressor impacts of malaria infection, food limitation, and 2,4,6-trinitrotoluene (TNT) exposures on gene expression in livers of Western fence lizard (WFL, Sceloporus occidentalis) using custom WFL transcriptome-based microarrays. Computational analysis including annotation enrichment and correlation analysis identified putative functional mechanisms between transcript expression and toxicological phenotype. TNT exposure increased transcript expression for genes involved in erythropoiesis, potentially in response to TNT-induced anemia and/or methemoglobinemia, and caused dose-specific effects on genes involved in lipid and overall energy metabolism consistent with a hormesis response of growth stimulation at low doses contrasted with adverse effects on lizard growth at high doses. Functional enrichment and inguinal fat body weights suggest inhibition of lipid mobilization and catabolism by TNT coupled with a decreased overall energy budget. Malaria infection elicited enrichment of the expression of multiple immune-related functions likely corresponding to increased white blood cell (WBC) counts. Food limitation alone enriched functions related to cellular energy production and decreased expression of immune response consistent with a decrease in WBC levels. Despite these findings, the lizards demonstrated immune resilience to malaria infection under food limitation with transcriptional results indicating a fully competent immune response to malaria, even under bioenergetic constraints. Interestingly, each TNT and malaria individually tended to increase transcriptional expression of immune-related genes and increase overall WBC concentrations in blood; responses that were retained in the TNT x malaria combined exposure. The results demonstrate complex and sometimes unexpected responses to multiple stressors where the lizards displayed remarkable resiliency to the stressor combinations investigated.

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Combining multiple stressors unexpectedly blocks bacterial migration and growth

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