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The phosphorylated regulator of chemotaxis is crucial throughout biofilm biogenesis in Shewanella oneidensis.

ABSTRACT: The core of the chemotaxis system of Shewanella oneidensis is made of the CheA3 kinase and the CheY3 regulator. When appropriated, CheA3 phosphorylates CheY3, which, in turn, binds to the rotor of the flagellum to modify the swimming direction. In this study, we showed that phosphorylated CheY3 (CheY3-P) also plays an essential role during biogenesis of the solid-surface-associated biofilm (SSA-biofilm). Indeed, in a ?cheY3 strain, the formation of this biofilm is abolished. Using the phospho-mimetic CheY3D56E mutant, we showed that CheY-P is required throughout the biogenesis of the biofilm but CheY3 phosphorylation is independent of CheA3 during this process. We have recently found that CheY3 interacts with two diguanylate cyclases (DGCs) and with MxdA, the c-di-GMP effector, probably triggering exopolysaccharide synthesis by the Mxd machinery. Here, we discovered two additional DGCs involved in SSA-biofilm development and showed that one of them interacts with CheY3. We therefore propose that CheY3-P acts together with DGCs to control SSA-biofilm formation. Interestingly, two orthologous CheY regulators complement the biofilm defect of a ?cheY3 strain, supporting the idea that biofilm formation could involve CheY regulators in other bacteria.

SUBMITTER: Boyeldieu A

PROVIDER: S-EPMC7666153 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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The phosphorylated regulator of chemotaxis is crucial throughout biofilm biogenesis in Shewanella oneidensis.

Boyeldieu Anne A Ali Chaouche Amine A Ba Moly M Honoré Flora Ambre FA Méjean Vincent V Jourlin-Castelli Cécile C

NPJ biofilms and microbiomes 20201113 1

The core of the chemotaxis system of Shewanella oneidensis is made of the CheA3 kinase and the CheY3 regulator. When appropriated, CheA3 phosphorylates CheY3, which, in turn, binds to the rotor of the flagellum to modify the swimming direction. In this study, we showed that phosphorylated CheY3 (CheY3-P) also plays an essential role during biogenesis of the solid-surface-associated biofilm (SSA-biofilm). Indeed, in a ΔcheY3 strain, the formation of this biofilm is abolished. Using the phospho-mi ...[more]

PMID: 33188190

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Project description:BACKGROUND: The Shewanella oneidensis MR-1 genome encodes a predicted orphan DNA-binding response regulator, SO2426. Previous studies with a SO2426-deficient MR-1 strain suggested a putative functional role for SO2426 in the regulation of iron acquisition genes, in particular, the siderophore (hydroxamate) biosynthesis operon so3030-3031-3032. To further investigate the functional role of SO2426 in iron homeostasis, we employed computational strategies to identify putative gene targets of SO2426 regulation and biochemical approaches to validate the participation of SO2426 in the control of siderophore biosynthesis in S. oneidensis MR-1. RESULTS: In silico prediction analyses revealed a single 14-bp consensus motif consisting of two tandem conserved pentamers (5'-CAAAA-3') in the upstream regulatory regions of 46 genes, which were shown previously to be significantly down-regulated in a so2426 deletion mutant. These genes included so3030 and so3032, members of an annotated siderophore biosynthetic operon in MR-1. Electrophoretic mobility shift assays demonstrated that the SO2426 protein binds to its motif in the operator region of so3030. A "short" form of SO2426, beginning with a methionine at position 11 (M11) of the originally annotated coding sequence for SO2426, was also functional in binding to its consensus motif, confirming previous 5' RACE results that suggested that amino acid M11 is the actual translation start codon for SO2426. Alignment of SO2426 orthologs from all sequenced Shewanella spp. showed a high degree of sequence conservation beginning at M11, in addition to conservation of a putative aspartyl phosphorylation residue and the helix-turn-helix (HTH) DNA-binding domain. Finally, the so2426 deletion mutant was unable to synthesize siderophores at wild-type rates upon exposure to the iron chelator 2,2'-dipyridyl. CONCLUSIONS: Collectively, these data support the functional characterization of SO2426 as a positive regulator of siderophore-mediated iron acquisition and provide the first insight into a coordinate program of multiple regulatory schemes controlling iron homeostasis in S. oneidensis MR-1.

Dataset Information

The phosphorylated regulator of chemotaxis is crucial throughout biofilm biogenesis in Shewanella oneidensis.

Publications

The phosphorylated regulator of chemotaxis is crucial throughout biofilm biogenesis in Shewanella oneidensis.

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