Agrobacterium tumefaciens ExoR represses succinoglycan biosynthesis and is required for biofilm formation and motility

Tomlinson, Amelia D.; Ramey-Hartung, Bronwyn; Day, Travis W.; Merritt, Peter M.; Fuqua, Clay

doi:10.1099/mic.0.039032-0

Cited by 63 publications

(74 citation statements)

References 51 publications

(80 reference statements)

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“…A diversity of Alphaproteobacteria have an ExoR homologue, including mammalian pathogens such as Brucella abortus and free-living bacteria such as Nitrobacter hamburgensis, in all cases with a well-supported N-terminal secretion signal and TPRs (18). A. tumefaciens has an ExoR homologue that is highly similar to that from S. meliloti, and A. tumefaciens exoR mutants derepress SCG production and lack flagella, due at least in part by the mutation affecting the transcription of exo and motility genes (18).…”

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confidence: 99%

“…A. tumefaciens has an ExoR homologue that is highly similar to that from S. meliloti, and A. tumefaciens exoR mutants derepress SCG production and lack flagella, due at least in part by the mutation affecting the transcription of exo and motility genes (18). In contrast to S. meliloti, an A. tumefaciens exoR mutant was isolated by virtue of its inability to form biofilms (18).…”

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confidence: 99%

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Agrobacterium tumefaciens ExoR Controls Acid Response Genes and Impacts Exopolysaccharide Synthesis, Horizontal Gene Transfer, and Virulence Gene Expression

et al. 2014

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bAgrobacterium tumefaciens is a facultative plant pathogen and the causative agent of crown gall disease. The initial stage of infection involves attachment to plant tissues, and subsequently, biofilms may form at these sites. This study focuses on the periplasmic ExoR regulator, which was identified based on the severe biofilm deficiency of A. tumefaciens exoR mutants. Genome-wide expression analysis was performed to elucidate the complete ExoR regulon. Overproduction of the exopolysaccharide succinoglycan is a dramatic phenotype of exoR mutants. Comparative expression analyses revealed that the core ExoR regulon is unaffected by succinoglycan synthesis. Several findings are consistent with previous observations: genes involved in succinoglycan biosynthesis, motility, and type VI secretion are differentially expressed in the ⌬exoR mutant. In addition, these studies revealed new functional categories regulated by ExoR, including genes related to virulence, conjugation of the pAtC58 megaplasmid, ABC transporters, and cell envelope architecture. To address how ExoR exerts a broad impact on gene expression from its periplasmic location, a genetic screen was performed to isolate suppressor mutants that mitigate the exoR motility phenotype and identify downstream components of the ExoR regulatory pathway. This suppression analysis identified the acidsensing two-component system ChvG-ChvI, and the suppressor mutant phenotypes suggest that all or most of the characteristic exoR properties are mediated through ChvG-ChvI. Subsequent analysis indicates that exoR mutants are simulating a response to acidic conditions, even in neutral media. This work expands the model for ExoR regulation in A. tumefaciens and underscores the global role that this regulator plays on gene expression.

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Agrobacterium tumefaciens ExoR Controls Acid Response Genes and Impacts Exopolysaccharide Synthesis, Horizontal Gene Transfer, and Virulence Gene Expression

et al. 2014

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“…The direct role of ChvG/ChvI in regulation of succinoglycan in A. tumefaciens has not been reported. However, mutation of exoR, a periplasmic protein that inhibits ChvG, results in hypermucoid cells in A. tumefaciens strain C58, providing indirect evidence that ChvG and ChvI regulate succinoglycan production in A. tumefaciens (36). R. leguminosarum strains do not produce succinoglycan or galactoglucan.…”

Section: Resultsmentioning

confidence: 99%

“…Both A. tumefaciens and S. meliloti produce the exopolysaccharide succinoglycan in a manner dependent on the presence of functional ChvG (ExoS)/ChvI (2,7,36). Null mutants of exoS and chvI in S. meliloti do not produce succinoglycan (2).…”

Section: Discussionmentioning

confidence: 99%

Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis

Vanderlinde

Yost

2012

J Bacteriol

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Two-component signal transduction systems (TCS) are a main strategy used by bacteria to sense and adapt to changes in their environment. In the legume symbiont Rhizobium leguminosarum biovar viciae VF39, mutation of chvG, a histidine kinase, caused a number of pleiotropic phenotypes. ChvG mutants are unable to grow on proline, glutamate, histidine, or arginine as the sole carbon source. The chvG mutant secreted smaller amounts of acidic and neutral surface polysaccharides and accumulated abnormally large amounts of poly-ß-hydroxybutyrate. Mutation of chvG caused symbiotic defects on peas, lentils, and vetch; nodules formed by the chvG mutant were small and white and contained only a few cells that had failed to differentiate into bacteroids. Mutation of chvG also destabilized the outer membrane of R. leguminosarum, resulting in increased sensitivity to membrane stressors. Constitutive expression of ropB, the outer membrane protein-encoding gene, restored membrane stability and rescued the sensitivity phenotypes described above. Similar phenotypes have been described for mutations in other ChvG-regulated genes encoding a conserved operon of unknown function and in the fabXL genes required for synthesis of the lipid A very-long-chain fatty acid, suggesting that ChvG is a key component of the envelope stress response in Rhizobium leguminosarum. Collectively, the results of this study demonstrate the important and unique role the ChvG/ChvI TCS plays in the physiology, metabolism, and symbiotic competency of R. leguminosarum.

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“…This activity of this system is repressed at neutral pH because of periplasmic interactions between ExoR and the sensor kinase ChvG (99). ExoR is a periplasmic protein containing tetratricopeptide repeats (100). Derepression of ChvG leads to phosphorylation of ChvI and, surprisingly, the reduction of both motility and biofilm formation.…”

Section: Surface Sensing and Signal Transductionmentioning

confidence: 99%

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

et al. 2017

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The structure and function of two-component and chemotactic signaling and different aspects related to the motility of bacteria and archaea are key research areas in modern microbiology. Escherichia coli is the traditional model organism used to study chemotaxis signaling and motility. However, the recent study of a wide range of bacteria and even some archaea with different lifestyles has provided new insight into the ecophysiology of chemotaxis, which is essential for the establishment of different pathogens or beneficial bacteria in a host. The expanded range of model organisms has also permitted the study of chemosensory pathways unrelated to chemotaxis, multiple chemotaxis pathways within an organism, and new types of chemoreceptors. This research has greatly benefitted from technical advances in the field of cryomicroscopy, which continues to reveal with increasing resolution the complexity and diversity of large protein complexes like the flagellar motor or chemoreceptor arrays. In addition, sensitive instruments now allow an increasing number of experiments to be conducted at the single-cell level, thereby revealing information that is beginning to bridge the gap between individual cells and population behavior. Evidence has also accumulated showing that bacteria have evolved different mechanisms for surface sensing, which appears to be mediated by flagella and possibly type IV pili, and that the downstream signaling involves chemosensory pathways and two-component-system-based processes. Herein, we summarize the recent advances and research tendencies in this field as presented at the latest Bacterial Locomotion and Signal Transduction (BLAST XIV) conference.KEYWORDS chemotaxis, flagella, flagellar motility, signal transduction, two-component regulatory systems T he capacity to sense and respond to changes in environmental cues is an essential feature of the prokaryotic lifestyle. As a consequence, bacteria and archaea have evolved an array of different molecular mechanisms that permit the detection of signals in order to generate appropriate cellular responses. These responses are mediated primarily by one-and two-component systems, as well as chemosensory signaling pathways (1-4). Whereas the former systems mediate changes primarily at the transcriptional level, chemosensory pathways form the basis for chemotaxis, the directed movement of prokaryotes in compound gradients. The study of signaling processes is not only of fundamental interest but may also contribute to the tackling of one of the central clinical problems, which is the increasing amount of antibiotic-resistant pathogens. There is now a significant amount of data indicating that interference with signal transduction systems, motility, and chemotaxis can be an alternative strategy to weaken or block pathogens (5, 6).In

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Agrobacterium tumefaciens ExoR represses succinoglycan biosynthesis and is required for biofilm formation and motility

Cited by 63 publications

References 51 publications

Agrobacterium tumefaciens ExoR Controls Acid Response Genes and Impacts Exopolysaccharide Synthesis, Horizontal Gene Transfer, and Virulence Gene Expression

Agrobacterium tumefaciens ExoR Controls Acid Response Genes and Impacts Exopolysaccharide Synthesis, Horizontal Gene Transfer, and Virulence Gene Expression

Mutation of the Sensor Kinase chvG in Rhizobium leguminosarum Negatively Impacts Cellular Metabolism, Outer Membrane Stability, and Symbiosis

Recent Advances and Future Prospects in Bacterial and Archaeal Locomotion and Signal Transduction

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