Dataset Information

Responses to elevated c-di-GMP levels in mutualistic and pathogenic plant-interacting bacteria.

ABSTRACT: Despite a recent burst of research, knowledge on c-di-GMP signaling pathways remains largely fragmentary and molecular mechanisms of regulation and even c-di-GMP targets are yet unknown for most bacteria. Besides genomics or bioinformatics, accompanying alternative approaches are necessary to reveal c-di-GMP regulation in bacteria with complex lifestyles. We have approached this study by artificially altering the c-di-GMP economy of diverse pathogenic and mutualistic plant-interacting bacteria and examining the effects on the interaction with their respective host plants. Phytopathogenic Pseudomonas and symbiotic Rhizobium strains with enhanced levels of intracellular c-di-GMP displayed common free-living responses: reduction of motility, increased production of extracellular polysaccharides and enhanced biofilm formation. Regarding the interaction with the host plants, P. savastanoi pv. savastanoi cells containing high c-di-GMP levels formed larger knots on olive plants which, however, displayed reduced necrosis. In contrast, development of disease symptoms in P. syringae-tomato or P. syringae-bean interactions did not seem significantly affected by high c-di-GMP. On the other hand, increasing c-di-GMP levels in symbiotic R. etli and R. leguminosarum strains favoured the early stages of the interaction since enhanced adhesion to plant roots, but decreased symbiotic efficiency as plant growth and nitrogen contents were reduced. Our results remark the importance of c-di-GMP economy for plant-interacting bacteria and show the usefulness of our approach to reveal particular stages during plant-bacteria associations which are sensitive to changes in c-di-GMP levels.

SUBMITTER: Perez-Mendoza D

PROVIDER: S-EPMC3953490 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Responses to elevated c-di-GMP levels in mutualistic and pathogenic plant-interacting bacteria.

Pérez-Mendoza Daniel D Aragón Isabel M IM Prada-Ramírez Harold A HA Romero-Jiménez Lorena L Ramos Cayo C Gallegos María-Trinidad MT Sanjuán Juan J

PloS one 20140313 3

Despite a recent burst of research, knowledge on c-di-GMP signaling pathways remains largely fragmentary and molecular mechanisms of regulation and even c-di-GMP targets are yet unknown for most bacteria. Besides genomics or bioinformatics, accompanying alternative approaches are necessary to reveal c-di-GMP regulation in bacteria with complex lifestyles. We have approached this study by artificially altering the c-di-GMP economy of diverse pathogenic and mutualistic plant-interacting bacteria a ...[more]

PMID: 24626229

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Project description:Bacterial chemotaxis receptors provide the sensory inputs that inform the direction of navigation in changing environments. Recently, we described the bacterial second messenger cyclic di-GMP (c-di-GMP) as a novel regulator of a subclass of chemotaxis receptors. In Azospirillum brasilense, c-di-GMP binds to a chemotaxis receptor, Tlp1, and modulates its signaling function during aerotaxis. Here, we further characterize the role of c-di-GMP in aerotaxis using a novel dichromatic optogenetic system engineered for manipulating intracellular c-di-GMP levels in real time. This system comprises a red/near-infrared-light-regulated diguanylate cyclase and a blue-light-regulated c-di-GMP phosphodiesterase. It allows the generation of transient changes in intracellular c-di-GMP concentrations within seconds of irradiation with appropriate light, which is compatible with the time scale of chemotaxis signaling. We provide experimental evidence that binding of c-di-GMP to the Tlp1 receptor activates its signaling function during aerotaxis, which supports the role of transient changes in c-di-GMP levels as a means of adjusting the response of A. brasilense to oxygen gradients. We also show that intracellular c-di-GMP levels in A. brasilense change with carbon metabolism. Our data support a model whereby c-di-GMP functions to imprint chemotaxis receptors with a record of recent metabolic experience, to adjust their contribution to the signaling output, thus allowing the cells to continually fine-tune chemotaxis sensory perception to their metabolic state.IMPORTANCE Motile bacteria use chemotaxis to change swimming direction in response to changes in environmental conditions. Chemotaxis receptors sense environmental signals and relay sensory information to the chemotaxis machinery, which ultimately controls the swimming pattern of cells. In bacteria studied to date, differential methylation has been known as a mechanism to control the activity of chemotaxis receptors and modulates their contribution to the overall chemotaxis response. Here, we used an optogenetic system to perturb intracellular concentrations of the bacterial second messenger c-di-GMP to show that in some chemotaxis receptors, c-di-GMP functions in a similar feedback loop to connect the metabolic status of the cells to the sensory activity of chemotaxis receptors.

Project description:BackgroundMicrobe-virus interactions have broad implications on the composition, function, and evolution of microbiomes. Elucidating the effects of environmental stresses on these interactions is critical to identify the ecological function of viral communities and understand microbiome environmental adaptation. Heavy metal-contaminated soils represent a relevant ecosystem to study the interplay between microbes, viruses, and environmental stressors.ResultsMetagenomic analysis revealed that Cr pollution adversely altered the abundance, diversity, and composition of viral and bacterial communities. Host-phage linkage based on CRISPR indicated that, in soils with high Cr contamination, the abundance of phages associated with heavy metal-tolerant hosts increased, as did the relative abundance of phages with broad host ranges (identified as host-phage linkages across genera), which would facilitate transfection and broader distribution of heavy metal resistance genes in the bacterial community. Examining variations along the pollutant gradient, enhanced mutualistic phage-bacterium interactions were observed in the face of greater environmental stresses. Specifically, the fractions of lysogens in bacterial communities (identified by integrase genes within bacterial genomes and prophage induction assay by mitomycin-C) were positively correlated with Cr contamination levels. Furthermore, viral genomic analysis demonstrated that lysogenic phages under higher Cr-induced stresses carried more auxiliary metabolic genes regulating microbial heavy metal detoxification.ConclusionWith the intensification of Cr-induced environmental stresses, the composition, replication strategy, and ecological function of the phage community all evolve alongside the bacterial community to adapt to extreme habitats. These result in a transformation of the phage-bacterium interaction from parasitism to mutualism in extreme environments and underscore the influential role of phages in bacterial adaptation to pollution-related stress and in related biogeochemical processes. Video Abstract.

Dataset Information

Responses to elevated c-di-GMP levels in mutualistic and pathogenic plant-interacting bacteria.

Publications

Responses to elevated c-di-GMP levels in mutualistic and pathogenic plant-interacting bacteria.

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