The Cyclic Adenosine Monophosphate Phosphodiesterase CpdA Modulates cAMP Homeostasis, Stress Adaptability, Biofilm Formation, Motility, Quorum Sensing and Antibiotic Resistance of Aeromonas veronii

环磷酸腺苷磷酸二酯酶CpdA调节维罗尼气单胞菌的cAMP稳态、应激适应性、生物膜形成、运动性、群体感应和抗生素耐药性

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Abstract

Aeromonas veronii, a Gram-negative pathogen, is ubiquitous in nature and infects broad hosts, which becomes a serious threat to the public health. The cyclic adenosine monophosphate (cAMP), precisely modulated by cyclic nucleotide phosphodiesterase (PDE), regulates key cellular processes in bacteria. However, the specific function and regulatory role of PDE in A. veronii remain unclear. In this study, a Class III PDE gene named as cpdA in A. veronii WL-3 was identified for the first time, which shared 39.18%-49.19% identity with homologs from other bacteria and also contained the conserved metal-binding motif. For functional elucidation, a cpdA-deleted mutant WL-3ΔcpdA was constructed. The results showed that the intracellular cAMP level in WL-3ΔcpdA was 2.34-fold higher than that in WL-3, confirming the PDE activity in vivo. WL-3ΔcpdA exhibited impaired growth under the normal condition and reduced tolerance to NaCl and pH stresses. Furthermore, the deficiency of cpdA significantly inhibited biofilm formation and swimming motility, which were consistent with aberrant flagellar structure and decreased N-acyl-homoserine lactone production. In contrast, the expression of nine flagella-related genes and two quorum-sensing genes was upregulated. Interestingly, WL-3ΔcpdA conferred higher resistance to partial β-lactam antibiotics with upregulation of bla(CphA3) and bla(OXA-12), but heightened sensitivity to kanamycin, neomycin, polymyxin B, and erythromycin, positioning CpdA as a multifaceted effector. Genetic complementation partially or fully reversed the most defects of WL-3ΔcpdA. These results identify that CpdA is involved in regulating various physiological properties of A. veronii, thus nominating CpdA as an attractive and novel target for anti-infective strategies.

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