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

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Τίτλος: Growth mode-dependent proteomic responses of Bacillus subtilis to cerium oxide nanoparticles: Pellicle biofilm versus swarming.
Συγγραφείς: Darrouzet E; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: elisabeth.darrouzet@cea.fr., Luche S; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: sylvie.luche@cea.fr., Diemer H; Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC UMR 7178, Université de Strasbourg, CNRS, 67087 Strasbourg, France; Infrastructure Nationale de Protéomique ProFI - FR2048, 67087 Strasbourg, France. Electronic address: hdiemer@unistra.fr., Cianférani S; Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC UMR 7178, Université de Strasbourg, CNRS, 67087 Strasbourg, France; Infrastructure Nationale de Protéomique ProFI - FR2048, 67087 Strasbourg, France. Electronic address: sarah.cianferani@unistra.fr., Lafond-Fenonjoie D; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France., Rabilloud T; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: thierry.rabilloud@cnrs.fr., Lelong C; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: cecile.lelong@univ-grenoble-alpes.fr.
Πηγή: Journal of proteomics [J Proteomics] 2026 Aug 15; Vol. 330, pp. 105696. Date of Electronic Publication: 2026 Jun 09.
Τύπος έκδοσης: Journal Article
Γλώσσα: English
Στοιχεία περιοδικού: Publisher: Elsevier Country of Publication: Netherlands NLM ID: 101475056 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1876-7737 (Electronic) Linking ISSN: 18743919 NLM ISO Abbreviation: J Proteomics Subsets: MEDLINE
Imprint Name(s): Original Publication: Amsterdam : Elsevier
Ιατρικοί όροι (MeSH): Bacillus subtilis*/metabolism , Bacillus subtilis*/growth & development , Bacillus subtilis*/drug effects , Bacillus subtilis*/physiology , Cerium*/pharmacology , Biofilms*/growth & development , Biofilms*/drug effects , Bacterial Proteins*/metabolism , Proteome*/metabolism , Nanoparticles* , Metal Nanoparticles*, Proteomics/methods ; Oxidative Stress/drug effects
Περίληψη: 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.
(Copyright © 2026 Elsevier B.V. All rights reserved.)
Competing Interests: Declaration of competing interest The authors declare that they have no competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Contributed Indexing: Keywords: Bacillus subtilis; Biofilm; Nanoparticle; Swarming
Substance Nomenclature: 30K4522N6T (Cerium)
619G5K328Y (ceric oxide)
0 (Bacterial Proteins)
0 (Proteome)
Entry Date(s): Date Created: 20260609 Date Completed: 20260716 Latest Revision: 20260716
Update Code: 20260717
DOI: 10.1016/j.jprot.2026.105696
PMID: 42264144
Βάση Δεδομένων: MEDLINE
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  Data: Growth mode-dependent proteomic responses of Bacillus subtilis to cerium oxide nanoparticles: Pellicle biofilm versus swarming.
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  Data: <searchLink fieldCode="AU" term="%22Darrouzet+E%22">Darrouzet E</searchLink>; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: elisabeth.darrouzet@cea.fr.<br /><searchLink fieldCode="AU" term="%22Luche+S%22">Luche S</searchLink>; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: sylvie.luche@cea.fr.<br /><searchLink fieldCode="AU" term="%22Diemer+H%22">Diemer H</searchLink>; Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC UMR 7178, Université de Strasbourg, CNRS, 67087 Strasbourg, France; Infrastructure Nationale de Protéomique ProFI - FR2048, 67087 Strasbourg, France. Electronic address: hdiemer@unistra.fr.<br /><searchLink fieldCode="AU" term="%22Cianférani+S%22">Cianférani S</searchLink>; Laboratoire de Spectrométrie de Masse BioOrganique (LSMBO), IPHC UMR 7178, Université de Strasbourg, CNRS, 67087 Strasbourg, France; Infrastructure Nationale de Protéomique ProFI - FR2048, 67087 Strasbourg, France. Electronic address: sarah.cianferani@unistra.fr.<br /><searchLink fieldCode="AU" term="%22Lafond-Fenonjoie+D%22">Lafond-Fenonjoie D</searchLink>; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France.<br /><searchLink fieldCode="AU" term="%22Rabilloud+T%22">Rabilloud T</searchLink>; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: thierry.rabilloud@cnrs.fr.<br /><searchLink fieldCode="AU" term="%22Lelong+C%22">Lelong C</searchLink>; Univ Grenoble Alpes, CEA, CNRS, IRIG, Laboratoire de Chimie et Biologie des Métaux, 17 rue des Martyrs, 38000 Grenoble, France. Electronic address: cecile.lelong@univ-grenoble-alpes.fr.
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  Label: Abstract
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  Data: 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.<br /> (Copyright © 2026 Elsevier B.V. All rights reserved.)
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  Data: Declaration of competing interest The authors declare that they have no competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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  Data: <i>Keywords: </i>Bacillus subtilis; Biofilm; Nanoparticle; Swarming
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  Data: 30K4522N6T (Cerium)<br />619G5K328Y (ceric oxide)<br />0 (Bacterial Proteins)<br />0 (Proteome)
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        Value: 10.1016/j.jprot.2026.105696
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        Text: English
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        Type: general
      – SubjectFull: Oxidative Stress drug effects
        Type: general
      – SubjectFull: Bacillus subtilis metabolism
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      – TitleFull: Growth mode-dependent proteomic responses of Bacillus subtilis to cerium oxide nanoparticles: Pellicle biofilm versus swarming.
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