Oxygen-selective regulation of cyclic di-GMP synthesis by a globin coupled sensor with a shortened linking domain modulates Shewanella sp. ANA-3 biofilm

• Published in: Journal of inorganic biochemistry 2024-03, Vol.252, p.112482, Article 112482
• Main Authors: Schuelke-Sanchez, Ariel, Yennawar, Neela H., Weinert, Emily E.
• Format: Article
• Language: English
• Subjects: Bacterial Proteins - chemistry; Biofilm; Biofilms; Cyclic GMP - analogs & derivatives; Diguanylate cyclase; Escherichia coli Proteins - chemistry; Globin; Globins - chemistry; Heme; Heme - chemistry; Oxygen - metabolism; Oxygen sensing; Phosphorus-Oxygen Lyases - chemistry; Shewanella
• ISSN: 0162-0134; 1873-3344; 1873-3344
• DOI: 10.1016/j.jinorgbio.2024.112482

Bacteria utilize heme proteins, such as globin coupled sensors (GCSs), to sense and respond to oxygen levels. GCSs are predicted in almost 2000 bacterial species and consist of a globin domain linked by a central domain to a variety of output domains, including diguanylate cyclase domains that synthesize c-di-GMP, a major regulator of biofilm formation. To investigate the effects of middle domain length and heme edge residues on GCS diguanylate cyclase activity and cellular function, a putative diguanylate cyclase-containing GCS from Shewanella sp. ANA-3 (SA3GCS) was characterized. Binding of O2 to the heme resulted in activation of diguanylate cyclase activity, while NO and CO binding had minimal effects on catalysis, demonstrating that SA3GCS exhibits greater ligand selectivity for cyclase activation than many other diguanylate cyclase-containing GCSs. Small angle X-ray scattering analysis of dimeric SA3GCS identified movement of the cyclase domains away from each other, while maintaining the globin dimer interface, as a potential mechanism for regulating cyclase activity. Comparison of the Shewanella ANA-3 wild type and SA3GCS deletion (ΔSA3GCS) strains identified changes in biofilm formation, demonstrating that SA3GCS diguanylate cyclase activity modulates Shewanella phenotypes. The globin coupled sensor from Shewanella sp. ANA-3 exhibits O2-selective diguanylate cyclase activity, which is controlled by conformational changes, and modulates biofilm formation. [Display omitted] •Globin coupled sensor middle domain correlates with O2 selective cyclase activation.•Heme edge tyrosine residue involved in rapid O2 dissociation.•Deletion of the globin coupled sensor results in decreased biofilm formation.