Schmidt William C, Lee Calvin K, Zheng Xuhui, Chen Jonathan W, Fetah Kirsten L, Popoli James R, Choi Yun Su, Young Thomas D, Weiss Paul S, Kasko Andrea M, O'Toole George A, Parsek Matthew R, Wong Gerard C L
Department of Bioengineering, University of California, Los Angeles, Los Angeles, CA, USA.
Department of Chemistry and Biochemistry, University of California, Los Angeles, Los Angeles, CA, USA.
Nat Microbiol. 2025 Sep 5. doi: 10.1038/s41564-025-02087-4.
During early stages of biofilm formation, Pseudomonas aeruginosa (Pa) PAO1 can sense exopolysaccharide (EPS) trails of Psl deposited on a surface by previous Pa cells to detect trajectories of other cells and to orchestrate motility. This sensory signal is transduced into cyclic diGMP second messengers, but no known Psl receptors and adhesins participate in signal transduction. Here, using bacteria-secreted Psl trails, glycopolymer-patterned surfaces, longitudinal cell tracking, second messenger dual reporters and genetic mutations targeting EPS binding and surface twitching, we find that Pa is capable of sensing EPS directly through mutually constitutive interactions between type IV pili (T4P)-powered twitching and specific adhesin-EPS bonds. This unanticipated mechanochemical surveillance of the Pa environment, where T4P pull against cell-body localized adhesins interacting with EPS trails, such as mannose-binding CdrA, generates a hybrid, transitional planktonic-to-biofilm population with elevated cyclic diGMP and elevated cyclic AMP, as well as increased motility capable of following EPS trails. These results show a generalizable mechanism of surface chemosensing through mechanosensitive appendages.
在生物膜形成的早期阶段,铜绿假单胞菌(Pa)PAO1能够感知先前的Pa细胞沉积在表面的胞外多糖(EPS)Psl痕迹,以检测其他细胞的轨迹并协调运动。这种感官信号被转化为环二鸟苷酸第二信使,但目前尚不清楚有哪些Psl受体和粘附素参与信号转导。在此,我们利用细菌分泌的Psl痕迹、糖聚合物图案化表面、纵向细胞追踪、第二信使双报告基因以及针对EPS结合和表面颤动的基因突变,发现Pa能够通过IV型菌毛(T4P)驱动的颤动与特定粘附素-EPS键之间的相互组成性相互作用直接感知EPS。这种对Pa环境的意外机械化学监测中,T4P拉动与EPS痕迹相互作用的细胞体定位粘附素,如甘露糖结合CdrA,产生了一个具有升高的环二鸟苷酸和升高的环磷酸腺苷的混合性、过渡性浮游生物到生物膜群体,以及能够跟随EPS痕迹的增强运动能力。这些结果展示了一种通过机械敏感附属物进行表面化学传感的普遍机制。