<i>Xylella fastidiosa</i>
            outer membrane vesicles modulate plant colonization by blocking attachment to surfaces

Ionescu, Michael; Zaini, Paulo A.; Baccari, Clelia; Tran, Sophia; Silva, da; Lindow, Steven E.

doi:10.1073/pnas.1414944111

Cited by 132 publications

(145 citation statements)

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“…In line with this hypothesis, phytoplasmas, being obligate parasites of plant and insects, sense the environment and switch their metabolism accordingly. Despite obvious differences, a very recent pioneer study has proposed that the xylem-limited bacterium Xylella fastidiosa switches its life style from adhesive cells capable of insect transmission to an "exploratory" lifestyle for systemic spread within the plant by production of outer membrane vesicles (80). Interestingly, the release of these vesicles is suppressed by a diffusible signal factor-dependent quorum-sensing system (80).…”

Section: Discussionmentioning

confidence: 99%

Decreasing Global Transcript Levels over Time Suggest that Phytoplasma Cells Enter Stationary Phase during Plant and Insect Colonization

Pacifico

Galetto

Rashidi

et al. 2015

Appl Environ Microbiol

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To highlight different transcriptional behaviors of the phytoplasma in the plant and animal host, expression of 14 genes of "Candidatus Phytoplasma asteris," chrysanthemum yellows strain, was investigated at different times following the infection of a plant host (Arabidopsis thaliana) and two insect vector species (Macrosteles quadripunctulatus and Euscelidius variegatus). Target genes were selected among those encoding antigenic membrane proteins, membrane transporters, secreted proteins, and general enzymes. Transcripts were detected for all analyzed genes in the three hosts; in particular, those encoding the antigenic membrane protein Amp, elements of the mechanosensitive channel, and two of the four secreted proteins (SAP54 and TENGU) were highly accumulated, suggesting that they play important roles in phytoplasma physiology during the infection cycle. Most transcripts were present at higher abundance in the plant host than in the insect hosts. Generally, transcript levels of the selected genes decreased significantly during infection of A. thaliana and M. quadripunctulatus but were more constant in E. variegatus. Such decreases may be explained by the fact that only a fraction of the phytoplasma population was transcribing, while the remaining part was aging to a stationary phase. This strategy might improve long-term survival, thereby increasing the likelihood that the pathogen may be acquired by a vector and/or inoculated to a healthy plant. Phytoplasmas are wall-less plant-pathogenic bacteria, classified as "Candidatus Phytoplasma" spp. (1). They belong to the class Mollicutes and infect a wide variety of plants, causing heavy crop losses in many different countries (2). Phytoplasmas are phloem limited in the infected plant, and they cause severe symptoms (yellowing, dwarfism, and phyllody), often leading to plant death. They are transmitted by phloem-feeding Hemipteran vectors (leafhoppers, planthoppers, and psyllids) in a persistent propagative manner (3).Phytoplasmas are obligate parasites that depend on host cells for the uptake of essential compounds such as sugars, amino acids, ions, and nucleotide precursors (4). Consistent with this lifestyle, phytoplasmas have very small, A/T-rich genomes, ranging from 530 to 1,350 kb in size (5), that lack essential metabolic pathways, such as ATP synthesis. This genome condensation reflects the phytoplasma adaptation to nutrient-rich environments such as the plant phloem (6) and helps explain why these pathogens are not cultivable under axenic conditions (7).Although the pathogenicity mechanisms are still largely unclear, phytoplasmas influence plant metabolism both directly, through a set of membrane proteins acting as molecular carriers (6), and indirectly, through secretion of effector proteins (8,9). In vitro studies have also shown that phytoplasma immunodominant membrane proteins interact with vector proteins (10, 11) and plant proteins (12) and are subjected to strong positive selection (13-15). Moreover, phytoplasmas can modulate their genome express...

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Section: Discussionmentioning

confidence: 99%

Decreasing Global Transcript Levels over Time Suggest that Phytoplasma Cells Enter Stationary Phase during Plant and Insect Colonization

Pacifico

Galetto

Rashidi

et al. 2015

Appl Environ Microbiol

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“…On evolutionary time scales, public goods provided by OMVs may select for cooperative behavior, driving the establishment of mutualisms. Finally, we note that the preponderance of research has examined OMVs in the context of animal symbioses; to date, only a few studies have focused on OMV-plant interactions (23,(99)(100)(101)(102)(103). Extending the role of OMVs in the biology of other multicellular lineages is a budding area for future investigation.…”

Section: Resultsmentioning

confidence: 96%

“…In addition to providing stimulatory cues, bacteria may secrete OMVs to enhance and reinforce the physical structure of polymicrobial biofilms (21,22,50). Conversely, OMVs may enable bacterial cells to transition from sessile to planktonic lifestyles, as in the case of Xylella fastidiosa OMVs that inhibit attachment to plant cells (23). Ionescu et al hypothesize that this confers a potential dispersal benefit to bacteria.…”

Section: Being a Good Neighbor: Benefits Provided By Omvsmentioning

confidence: 99%

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Spheres of Hope, Packets of Doom: the Good and Bad of Outer Membrane Vesicles in Interspecies and Ecological Dynamics

Lynch

Alegado

2017

J Bacteriol

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Outer membrane vesicles (OMVs) are proteoliposome nanoparticles ubiquitously produced by Gram-negative bacteria. Typically bearing a composition similar to those of the outer membrane and periplasm of the cells from which they are derived, OMVs package an array of proteins, lipids, and nucleic acids. Once considered inconsequential by-products of bacterial growth, OMVs have since been demonstrated to mediate cellular stress relief, promote horizontal gene transfer and antimicrobial activity, and elicit metazoan inflammation. Recently, OMVs have gained appreciation as critical moderators of interorganismal dynamics. In this review, we focus on recent progress toward understanding the functions of OMVs with regard to symbiosis and ecological contexts, and we propose potential avenues for future OMV studies.

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“…Based on the recent discovery that plant colonization by X. fastidiosa subsp fastidiosa strain Temecula is likely modulated by OMVs (Ionescu et al, 2014), we analyzed the secretome of strain 9a5c. This approach led us to identify the secreted proteins via MS/MS.…”

Section: Discussionmentioning

confidence: 99%

The Antitoxin Protein of a Toxin-Antitoxin System from Xylella fastidiosa Is Secreted via Outer Membrane Vesicles

et al. 2016

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The Xylella fastidiosa subsp pauca strain 9a5c is a Gram-negative, xylem-limited bacterium that is able to form a biofilm and affects citrus crops in Brazil. Some genes are considered to be involved in biofilm formation, but the specific mechanisms involved in this process remain unknown. This limited understanding of how some bacteria form biofilms is a major barrier to our comprehension of the progression of diseases caused by biofilm-producing bacteria. Several investigations have shown that the toxin-antitoxin (TA) operon is related to biofilm formation. This operon is composed of a toxin with RNAse activity and its cognate antitoxin. Previous reports have indicated that the antitoxin is able to inhibit toxin activity and modulate the expression of the operon as well as other target genes involved in oxidative stress and mobility. In this study, we characterize a toxin-antitoxin system consisting of XfMqsR and XfYgiT, respectively, from X. fastidiosa subsp. pauca strain 9a5c. These proteins display a high similarity to their homologs in X. fastidiosa strain Temecula and a predicted tridimensional structure that is similar to MqsR-YgiT from Escherichia coli. The characterization was performed using in vitro assays such as analytical ultracentrifugation (AUC), size exclusion chromatography, isothermal titration calorimetry, and Western blotting. Using a fluorometric assay to detect RNAses, we demonstrated that XfMqsR is thermostable and can degrade RNA. XfMqsR is inhibited by XfYgiT, which interacts with its own promoter. XfYgiT is known to be localized in the intracellular compartment; however, we provide strong evidence that X. fastidiosa secretes wild-type XfYgiT into the extracellular environment via outer membrane vesicles, as confirmed by Western blotting and specific immunofluorescence labeling visualized by fluorescence microscopy. Taken together, our results characterize the TA system from X. fastidiosa strain 9a5c, and we also discuss the possible influence of wild-type XfYgiT in the cell.

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Xylella fastidiosa outer membrane vesicles modulate plant colonization by blocking attachment to surfaces

Cited by 132 publications

References 61 publications

Decreasing Global Transcript Levels over Time Suggest that Phytoplasma Cells Enter Stationary Phase during Plant and Insect Colonization

Decreasing Global Transcript Levels over Time Suggest that Phytoplasma Cells Enter Stationary Phase during Plant and Insect Colonization

Spheres of Hope, Packets of Doom: the Good and Bad of Outer Membrane Vesicles in Interspecies and Ecological Dynamics

The Antitoxin Protein of a Toxin-Antitoxin System from Xylella fastidiosa Is Secreted via Outer Membrane Vesicles

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