N-Acetylglucosamine-dependent biofilm formation in Pectobacterium atrosepticum is cryptic and activated by elevated c-di-GMP levels

Pérez-Mendoza, Daniel; Coulthurst, Sarah J.; Sanjuán, Juan; Salmond, George P. C.

doi:10.1099/mic.0.050450-0

Cited by 47 publications

(39 citation statements)

References 57 publications

(73 reference statements)

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“…exopolysaccharides | cyclic diguanylate | plant-microbe interactions I n bacteria the second messenger cyclic diguanylate (c-di-GMP) regulates the transition from a motile to a sedentary lifestyle, so that high concentrations enhance the production of extracellular matrix components, exopolysaccharides (EPSs), and proteins (1)(2)(3)(4)(5). The c-di-GMP is synthesized from two molecules of GTP by the action of diguanylate cyclases (DGCs) and is hydrolyzed to 5′-phosphoguanylyl-(3′-5′)-guanosine by specific phosphodiesterases.…”

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confidence: 99%

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

Pérez-Mendoza

Rodrı́guez-Carvajal

Romero-Jiménez

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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109

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An artificial increase of cyclic diguanylate (c-di-GMP) levels in Sinorhizobium meliloti 8530, a bacterium that does not carry known cellulose synthesis genes, leads to overproduction of a substance that binds the dyes Congo red and calcofluor. Sugar composition and methylation analyses and NMR studies identified this compound as a linear mixed-linkage (1→3)(1→4)-β-D-glucan (ML β-glucan), not previously described in bacteria but resembling ML β-glucans found in plants and lichens. This unique polymer is hydrolyzed by the specific endoglucanase lichenase, but, unlike lichenan and barley glucan, it generates a disaccharidic →4)-β-DGlcp-(1→3)-β-D-Glcp-(1→ repeating unit. A two-gene operon bgsBA required for production of this ML β-glucan is conserved among several genera within the order Rhizobiales, where bgsA encodes a glycosyl transferase with domain resemblance and phylogenetic relationship to curdlan synthases and to bacterial cellulose synthases. ML β-glucan synthesis is subjected to both transcriptional and posttranslational regulation. bgsBA transcription is dependent on the exopolysaccharide/quorum sensing ExpR/SinI regulatory system, and posttranslational regulation seems to involve allosteric activation of the ML β-glucan synthase BgsA by c-di-GMP binding to its C-terminal domain. To our knowledge, this is the first report on a linear mixed-linkage (1→3)(1→4)-β-glucan produced by a bacterium. The S. meliloti ML β-glucan participates in bacterial aggregation and biofilm formation and is required for efficient attachment to the roots of a host plant, resembling the biological role of cellulose in other bacteria.exopolysaccharides | cyclic diguanylate | plant-microbe interactions

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confidence: 99%

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

Pérez-Mendoza

Rodrı́guez-Carvajal

Romero-Jiménez

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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109

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“…The decreased virulence of D. dadantii was attributed to downregulation of T3SS-related genes and decreased secretion of pectate lyase by c-di-GMP (20). Similarly, a recent study demonstrated that high levels of c-di-GMP promote the activation of a biofilm-forming phenotype in Pectobacterium atrosepticum and positively regulate the expression of poly-␤-1,6-N-acetyl-D-glucosamine (PGA), an EPS essential for biofilm formation (71). In Xanthomonas campestris pv.…”

Section: Discussionmentioning

confidence: 99%

Cyclic Di-GMP Modulates the Disease Progression of Erwinia amylovora

et al. 2013

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The second messenger cyclic di-GMP (c-di-GMP) is a nearly ubiquitous intracellular signal molecule known to regulate various cellular processes, including biofilm formation, motility, and virulence. The intracellular concentration of c-di-GMP is inversely governed by diguanylate cyclase (DGC) enzymes and phosphodiesterase (PDE) enzymes, which synthesize and degrade c-di-GMP, respectively. The role of c-di-GMP in the plant pathogen and causal agent of fire blight disease Erwinia amylovora has not been studied previously. Here we demonstrate that three of the five predicted DGC genes in E. amylovora (edc genes, for Erwinia diguanylate cyclase), edcA, edcC, and edcE, are active diguanylate cyclases. We show that c-di-GMP positively regulates the secretion of the main exopolysaccharide in E. amylovora, amylovoran, leading to increased biofilm formation, and negatively regulates flagellar swimming motility. Although amylovoran secretion and biofilm formation are important for the colonization of plant xylem tissues and the development of systemic infections, deletion of the two biofilm-promoting DGCs increased tissue necrosis in an immature-pear infection assay and an apple shoot infection model, suggesting that c-di-GMP negatively regulates virulence. In addition, c-di-GMP inhibited the expression of hrpA, a gene encoding the major structural component of the type III secretion pilus. Our results are the first to describe a role for c-di-GMP in E. amylovora and suggest that downregulation of motility and type III secretion by c-di-GMP during infection plays a key role in the coordination of pathogenesis. Erwinia amylovora is the causal agent of fire blight and a devastating phytopathogen that infects plant species of the family Rosaceae, most notably apple and pear trees (1). E. amylovora can infect flowers, fruits, actively growing shoots, and rootstock crowns (2). During the primary infection via the flower (1), E. amylovora cells multiply rapidly on the stigma. Motility and free moisture are important factors in the subsequent dissemination of cells down the outside of the stigma to nectarthodes, which provide entry into the plant (3-5).Following flower infection, E. amylovora cells spread systemically through host vascular tissues and cortical parenchyma. The wilting symptoms of fire blight are the result of bacterial invasion, the secretion of extracellular polysaccharide (EPS), and the formation of biofilms within host xylem that plug these tubes, restricting water flow (6, 7). E. amylovora secretes two distinct EPSs, amylovoran and levan, both of which contribute to plant infection (6). Amylovoran is an acidic polysaccharide composed of repeating units of galactose and glucuronic acid (8-10), while levan is a homopolymer of fructose residues synthesized from sucrose by the secreted enzyme levansucrase (11). Biofilm formation by E. amylovora is required for effective colonization of host xylem tissues, the exit of pathogen cells from infected leaves into host stems, and systemic spread within trees (6, 7). The...

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“…Several factors to this effect have been reported; for example, Prithiviraj et al (36) demonstrated that the Arabidopsis systemic plant defense signaling molecule, salicylic acid, suppresses Pseudomonas aeruginosa virulence genes such as those involved in attachment and biofilm formation without limiting bacterial growth. Additionally, Pérez-Mendosa et al (33) showed that in vitro biofilm formation in P. atrosepticum is activated and elevated by another signaling molecule, c-di-GMP. These authors suggested that, in the environment, it is possible that c-di-GMP modulate biofilm formation in P. atrosepticum as a response to asyet-unidentified plant signals in the environment.…”

Section: Discussionmentioning

confidence: 99%

Colonization Patterns of an mCherry-Tagged Pectobacterium carotovorum subsp. brasiliense Strain in Potato Plants

Kubheka¹,

Coutinho²,

Moleleki³

et al. 2013

Phytopathology®

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Pectobacterium carotovorum subsp. brasiliense is a newly identified member of the potato soft rot enterobacteriaceae. The pathogenesis of this pathogen is still poorly understood. In this study, an mCherry-P. carotovorum subsp. brasiliense-tagged strain was generated to study P. carotovorum subsp. brasiliense-potato plant interactions. Prior to use, the tagged strain was evaluated for in vitro growth, plasmid stability, and virulence on potato tubers and shown to be similar to the wild type. Four potato cultivars were evaluated for stem-based resistance against P. carotovorum subsp. brasiliense. Confocal laser-scanning microscopy and in vitro viable cell counts showed that P. carotovorum subsp. brasiliense is able to penetrate roots of a susceptible potato cultivar as early as 12 h postinoculation and migrate upward into aerial stem parts. Due to the phenotypic differences observed between tolerant and susceptible cultivars, a comparison of P. carotovorum subsp. brasiliense colonization patterns in these cultivars was undertaken. In the susceptible cultivar, P. carotovorum subsp. brasiliense cells colonized the xylem tissue, forming "biofilm-like" aggregates that led to occlusion of some of the vessels. In contrast, in the tolerant cultivar, P. carotovorum subsp. brasiliense appeared as free-swimming planktonic cells with no specific tissue localization. This suggests that there are resistance mechanisms in the tolerant cultivar that limit aggregation of P. carotovorum subsp. brasiliense in planta and, hence, the lack of symptom development in this cultivar.Additional keyword: Dickeya.

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N-Acetylglucosamine-dependent biofilm formation in Pectobacterium atrosepticum is cryptic and activated by elevated c-di-GMP levels

Cited by 47 publications

References 57 publications

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

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

Cyclic Di-GMP Modulates the Disease Progression of Erwinia amylovora

Colonization Patterns of an mCherry-Tagged Pectobacterium carotovorum subsp. brasiliense Strain in Potato Plants

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