Cyclic di-GMP Signaling Links Biofilm Formation and Mn(II) Oxidation in Pseudomonas resinovorans

PIAZZA, AINELÉN; PARRA, L; CIANCIO CASALINI, LUCILA; SISTI, FEDERICO; FERNANDEZ, JULIETA; MALONE, JACOB; OTTADO, JORGELINA; SERRA, D.; GOTTIG, N.

mBio

American Society for Microbiology

Lugar: Washington; Año: 2022

Bioaugmentation of biological sand filters with Mn(II)-oxidizing bacteria(MOB) is used to increase the efficiency of Mn removal from groundwater. While thebiofilm-forming ability of MOB is important to achieve optimal Mn filtration, the regulatorylink between biofilm formation and Mn(II) oxidation remains unclear. Here,an environmental isolate of Pseudomonas resinovorans strain MOB-513 was used as amodel to investigate the role of c-di-GMP, a second messenger crucially involved inthe regulation of biofilm formation by Pseudomonas, in the oxidation of Mn(II). Anovel role for c-di-GMP in the upregulation of Mn(II) oxidation through induction ofthe expression of manganese-oxidizing peroxidase enzymes was revealed. MOB-513macrocolony biofilms showed a strikingly stratified pattern of biogenic Mn oxide(BMnOx) accumulation in a localized top layer. Remarkably, elevated cellular levels ofc-di-GMP correlated not only with increased accumulation of BMnOx in the sametop layer but also with the appearance of a second BMnOx stratum in the bottomregion of macrocolony biofilms, and the expression of mop genes correlated withthis pattern. Proteomic analysis under Mn(II) conditions revealed changes in theabundance of a PilZ domain protein. Subsequent analyses supported a model inwhich this protein sensed c-di-GMP and affected a regulatory cascade that ultimatelyinhibited mop gene expression, providing a molecular link between c-di-GMP signalingand Mn(II) oxidation. Finally, we observed that high c-di-GMP levels were correlatedwith higher lyophilization efficiencies and higher groundwater Mn(II) oxidationcapacities of freeze-dried bacterial cells, named lyophiles, showing the biotechnologicalrelevance of understanding the role of c-di-GMP in MOB-513.