Local c-di-GMP Signaling in the Control of Synthesis of the E. coli Biofilm Exopolysaccharide pEtN-Cellulose
| Autor: | Nadezhda Malysheva, Anja M. Richter, Regine Hengge, Alexandra Possling, Kaveh Pouran Yousef, Susanne Herbst, Max von Kleist |
|---|---|
| Jazyk: | angličtina |
| Rok vydání: | 2020 |
| Předmět: |
bacterial second messenger
PDE phosphodiesterase Protein subunit Allosteric regulation AC adenylate cyclase medicine.disease_cause cellulose synthase Article GGDEF domain 03 medical and health sciences chemistry.chemical_compound 0302 clinical medicine Structural Biology medicine CR Congo red Cellulose Molecular Biology Escherichia coli Cyclic GMP 030304 developmental biology DGC diguanylate cyclase 0303 health sciences MSP membrane scaffold protein ATP synthase biology Escherichia coli K12 Phosphoric Diester Hydrolases Escherichia coli Proteins c-di-GMP bis-(3′–5′)-cyclic diguanosine monophosphate Polysaccharides Bacterial Intracellular Signaling Peptides and Proteins 3. Good health chemistry Biochemistry Glucosyltransferases Biofilms Second messenger system biology.protein pEtN phosphoethanolamine Diguanylate cyclase diguanylate cyclase Phosphorus-Oxygen Lyases 030217 neurology & neurosurgery Signal Transduction |
| Zdroj: | Journal of Molecular Biology |
| ISSN: | 1089-8638 0022-2836 |
| Popis: | In many bacteria, the biofilm-promoting second messenger c-di-GMP is produced and degraded by multiple diguanylate cyclases (DGC) and phosphodiesterases (PDE), respectively. High target specificity of some of these enzymes has led to theoretical concepts of “local” c-di-GMP signaling. In Escherichia coli K-12, which has 12 DGCs and 13 PDEs, a single DGC, DgcC, is specifically required for the biosynthesis of the biofilm exopolysaccharide pEtN-cellulose without affecting the cellular c-di-GMP pool, but the mechanistic basis of this target specificity has remained obscure. DGC activity of membrane-associated DgcC, which is demonstrated in vitro in nanodiscs, is shown to be necessary and sufficient to specifically activate cellulose biosynthesis in vivo. DgcC and a particular PDE, PdeK (encoded right next to the cellulose operon), directly interact with cellulose synthase subunit BcsB and with each other, thus establishing physical proximity between cellulose synthase and a local source and sink of c-di-GMP. This arrangement provides a localized, yet open source of c-di-GMP right next to cellulose synthase subunit BcsA, which needs allosteric activation by c-di-GMP. Through mathematical modeling and simulation, we demonstrate that BcsA binding from the low cytosolic c-di-GMP pool in E. coli is negligible, whereas a single c-di-GMP molecule that is produced and released in direct proximity to cellulose synthase increases the probability of c-di-GMP binding to BcsA several hundred-fold. This local c-di-GMP signaling could provide a blueprint for target-specific second messenger signaling also in other bacteria where multiple second messenger producing and degrading enzymes exist. Graphical abstract Unlabelled Image Highlights • The diguanylate cyclase DgcC specifically activates cellulose synthase in E. coli, without affecting the low cellular c-di-GMP pool and despite the presence of several other active diguanylate cyclases. • DgcC and a specific phosphodiesterase, PdeK, directly interact with the cellulose synthase complex. • DgcC and PdeK operate as a local c-di-GMP source and sink, respectively, right next to the c-di-GMP-binding cellulose synthase subunit BcsA in an open, non-compartmentalized system. • Mathematical modeling and simulation shows that this co-localization strongly increases the probability of c-di-GMP binding to BcsA and allows efficient signaling. |
| Databáze: | OpenAIRE |
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