Cyclic di-GMP signaling links biofilm formation and Mn(II) oxidation in Pseudomonas resinovorans

Piazza, Ainelén, Parra, Lucia, Ciancio Casalini, Lucila, Sisti, Federico, Fernández, Julieta, Malone, Jacob G. ORCID: https://orcid.org/0000-0003-1959-6820, Ottado, Jorgelina, Serra, Diego O. and Gottig, Natalia (2022) Cyclic di-GMP signaling links biofilm formation and Mn(II) oxidation in Pseudomonas resinovorans. mBIO, 13 (6). ISSN 2150-7511

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Abstract

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

Item Type: Article
Additional Information: Funding Information: The research performed in Argentina was supported by ANPCyT and CONICET. ANPCyT provided funding through PICT2019-01081 (to N.G.) and PICT2017-0240 (to D.O.S.) grants, and CONICET through PIP-1516 (to N.G.) grant. The experiments in J.G.M.’s lab, in the UK, were supported by the BBSRC grants: BBS/E/J/000PR9797 and BB/T004363/1. A.P.’s short-research stay abroad was supported by the IUBMB Wood-Whelan Fellowship. A.P. and L.C.C. were fellows of CONICET; L.P. is a fellow of CONICET; and F.S., J.F., J.O., D.O.S., and N.G. are staff members of CONICET. A.P., D.O.S., and N.G. conceived and designed the experimental plan, with additional contributions from F.S., J.F., J.G.M., and J.O. Most of the experiments were performed by A.P., L.P., and L.C.C. with contributions to the macrocolony experiments from D.O.S. and N.G. A.P., D.O.S., and N.G. wrote the manuscript, proof-read by F.S., J.F., J.G.M., and J.O.
Uncontrolled Keywords: pseudomonas,biofilms,bioremediation,c-di-gmp,metal oxidation,microbiology,virology ,/dk/atira/pure/subjectarea/asjc/2400/2404
Faculty \ School: Faculty of Science > School of Biological Sciences
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Depositing User: LivePure Connector
Date Deposited: 04 Mar 2024 18:38
Last Modified: 06 Mar 2024 13:31
URI: https://ueaeprints.uea.ac.uk/id/eprint/94553
DOI: 10.1128/mbio.02734-22

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