Growth mode-dependent proteomic responses of Bacillus subtilis to cerium oxide nanoparticles: Pellicle biofilm versus swarming.

Fiche publication

Date publication

juin 2026

Journal

Journal of proteomics

Auteurs

Membres identifiés du Cancéropôle Est :
Dr CIANFERANI Sarah

Tous les auteurs :
Darrouzet E, Luche S, Diemer H, Cianférani S, Lafond-Fenonjoie D, Rabilloud T, Lelong C

Lien Pubmed

https://www.ncbi.nlm.nih.gov/pubmed/42264144

Résumé

Proteomic analysis revealed that Bacillus subtilis exhibits markedly different physiological adaptations under pellicle biofilm and swarming growth conditions, and that these lifestyles strongly influence the bacterial response to CeO₂ nanoparticles. In pellicle biofilms, proteins involved in respiration, amino acid acquisition, Mn/Fe uptake, and SUF-mediated iron‑sulfur cluster synthesis were upregulated, together with oxidative stress defense systems, indicating adaptation to microaerobic and heterogeneous biofilm conditions. In contrast, swarming cells displayed increased sporulation-associated processes and a stronger stringent response. Exposure to CeO₂ nanoparticles induced a pronounced response, particularly under swarming conditions, where central carbon metabolism enzymes were strongly repressed and stringent response pathways were reinforced. In biofilms, CeO₂ effects were more moderate, with limited metabolic perturbation and a slight stimulation of biofilm formation. The contrasting responses between lifestyles appear primarily linked to differences in metabolic state, oxidative stress physiology, and nanoparticle accessibility within the biofilm matrix rather than to direct nanoparticle toxicity alone. Overall, these findings demonstrate that nanoceria impacts B. subtilis physiology in a growth mode-dependent manner and highlight the importance of considering bacterial lifestyle when evaluating nanoparticle toxicity. SIGNIFICANCE: This research provides a biologically understanding of how Bacillus subtilis, an important bacterium for soil, plant, and animal health, adapts to environmental stress under more physiologically realistic growth conditions. Using shotgun proteomics, we demonstrated that pellicle biofilm and swarming lifestyles are associated with profoundly distinct physiological states, notably in metabolism, oxidative stress management, metal homeostasis, and developmental regulation. Extending this approach to exposure to cerium oxide nanoparticles (CeO₂ NPs), a widely distributed environmental nanomaterial, we showed that bacterial responses are strongly dependent on growth mode. Swarming cells exhibited pronounced metabolic repression and activation of stringent response pathways, whereas biofilms displayed more limited perturbations together with slight stimulation of biofilm formation. These contrasting responses appear to result primarily from lifestyle-dependent differences in metabolic activity, oxidative stress physiology, and nanoparticle accessibility within the biofilm matrix rather than from direct nanoparticle toxicity alone. Since regulatory toxicology frameworks such as REACH often overlook subtle physiological adaptations, this study highlights the importance of considering microbial lifestyle and physiological context when assessing the ecological risks of emerging chemicals and nanomaterials.