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.

Novel mixed-linkage β-glucan activated by c-di-GMP in Sinorhizobium meliloti

“…In cellulose-producing (Cel + ) bacteria, raising c-di-GMP intracellular levels (i.e., by overexpression of a DGC) triggers production of cellulose and other extracellular molecules (5,6,27). S. meliloti 8530 does not bear any of the known CS operons in its genome; however, overexpression of the DGC PleD* generated wrinkled and red-stained colonies in medium with Congo red (CR), in deep contrast to the wild-type colonies (SI Appendix, Fig.…”

Ca 2+ -Induced Two-Component System CvsSR Regulates the Type III Secretion System and the Extracytoplasmic Function Sigma Factor AlgU in Pseudomonas syringae pv. tomato DC3000

“…tomato DC3000 has the capability of producing the EPSs Psl, cellulose, and levan along with alginate (5). Psl and cellulose can inhibit swarming in P. syringae (45,46). The genes PSPTO_3529 to PSPTO_3539, which code for proteins that produce Psl, were not differentially expressed between the WT and the ΔcvsR strain, nor was there a ChIP-seq peak near these genes.…”

“…Increased EPS production, decreased flagellar motility, and decreased biosurfactant production all result in decreasing swarming motility in P. syringae (45,63). It should be noted that we did not investigate whether changes in biosurfactant production occur in P. syringae pv.…”

“…Cellulose production commonly correlates with increased c-di-GMP in P. syringae pv. tomato DC3000 (45,65). Increases in c-di-GMP decrease swarming motility in Pseudomonas (66).…”

Cyclic Di-GMP Regulates Multiple Cellular Functions in the Symbiotic Alphaproteobacterium Sinorhizobium meliloti

“…In Rhizobium etli and Rhizobium leguminosarum, overproduction of a heterologous DGC enhanced EPS production, biofilm formation, and adhesion to plant roots and decreased symbiotic efficiency and swimming motility (22). In Sinorhizobium meliloti 102F34, overproduction of the E. coli cdG-binding protein BdcA resulted in biofilm dispersal and enhanced motility, presumably by lowering intracellular cdG levels (23).…”