Biophysical insights into sugar-dependent medium acidification promoting YfaL protein-mediated Escherichia coli self-aggregation, biofilm formation and acid stress resistance

• Published in: Nanoscale 2024-09, Vol.16 (37), p.17567-17584
• Main Authors: Chekli, Yankel, Thiriet-Rupert, Stanislas, Caillet, Céline, Quilès, Fabienne, Le Cordier, Hélène, Deshayes, Emilie, Bardiaux, Benjamin, Pédron, Thierry, Titecat, Marie, Debarbieux, Laurent, Ghigo, Jean-Marc, Francius, Grégory, Duval, Jérôme F L, Beloin, Christophe
• Format: Article
• Language: English
• Subjects: Acid resistance; Acidification; Acids - chemistry; Bacterial Adhesion - drug effects; Biofilms; Biofilms - drug effects; Biofilms - growth & development; Coliforms; E coli; Environmental Sciences; Escherichia coli - drug effects; Escherichia coli - physiology; Escherichia coli Proteins - chemistry; Escherichia coli Proteins - metabolism; Hydrogen-Ion Concentration; Life Sciences; Proteins; Stress, Physiological; Sugar; Sugars - chemistry; Sugars - metabolism
• ISSN: 2040-3364; 2040-3372; 2040-3372
• DOI: 10.1039/d4nr01884b

The ability of bacteria to interact with their environment is crucial to form aggregates and biofilms, and develop a collective stress resistance behavior. Despite its environmental and medical importance, bacterial aggregation is poorly understood and mediated by few known adhesion structures. Here, we identified a new role for a surface-exposed protein, YfaL, which can self-recognize and induce bacterial autoaggregation. This process occurs only under acidic conditions generated during growth in the presence of fermentable sugars. These findings were supported by electrokinetic and atomic force spectroscopy measurements, which revealed changes in the electrostatic, hydrophobic, and structural properties of YfaL-decorated cell surface upon sugar consumption. Furthermore, YfaL-mediated autoaggregation promotes biofilm formation and enhances resistance to acid stress. The prevalence and conservation of YfaL in environmental and clinical suggest strong evolutionary selection for its function inside or outside the host. Overall, our results emphasize the importance of environmental parameters such as low pH as physicochemical cues influencing bacterial adhesion and aggregation, affecting and potentially other bacteria's resistance to environmental stress.