Manganese oxidation counteracts the deleterious effect of low temperatures on biofilm formation in Pseudomonas sp. MOB-449

CIANCIO CASALINI, LUCILA; PIAZZA, AINELÉN; MASOTTI, FIORELLA; GARAVAGLIA, BETIANA S; GOTTIG, NATALIA; OTTADO, JORGELINA

Frontiers in Molecular Biosciences

Frontiers

Año: 2022

2296-889X

Mn removal from groundwater by biological sand filter technology is negativelyimpacted by low temperatures inwinter periods. Therefore, the need to studyMn(II)-oxidizing bacteria (MOB) having the potential to oxidize Mn(II) and form biofilms atlow temperatures is imperative. These MOB can have potential as inocula for sandfilter bioaugmentation strategies to optimize Mn removal during winter periods.Wepreviously showed that a Pseudomonas sp. MOB-449 (MOB-449), isolated from aMn biofilter, oxidizes Mn(II) in a biofilm-dependent way at low temperatures. In thiswork, MOB-449 Mn(II) oxidation and growth capacities were evaluated underplanktonic and biofilm conditions at different temperatures. At 18°C, MOB-449showed enhanced biofilm formation due to the addition of Mn(II) to the mediumcorrelating with Mn(II) oxidation, compared to biofilms grown in control medium.Moreover, this enhancement on biofilm formation due to the addition of Mn(II) wasonly observed at 18°C. At this temperature, Mn(II) oxidation in membrane fractionscollected from biofilms was induced by uncoupling oxidative phosphorylation fromthe electron transport chain with 2,4-Dinitrophenol. In Pseudomonas, a role forc-type cytochrome in Mn(II) oxidation has been demonstrated. Accordingly,transcriptional profiles of all terminal oxidases genes found in MOB-449 showedan induction of cytochrome c terminal oxidases expression mediated by Mn(II)oxidation at 18°C. Finally, heme peroxidase activity assays and MS analysis revealedthat PetC, a cytochrome c5, and also CcmE, involved in the cytochrome cbiogenesis machinery, are induced at 18°C only in the presence of Mn(II). Theseresults present evidence supporting that cytochromes c and also the cytochrome cterminal oxidases are activated at low temperatures in the presence ofMn(II).Overall,this work demonstrate that in MOB-449 Mn(II) oxidation is activated at lowtemperatures to gain energy, suggesting that this process is important forsurvival under adverse environmental conditions and contributing to theunderstanding of the physiological role of bacterial Mn(II) oxidation.