Protective plant immune responses are elicited by bacterial outer membrane vesicles.

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2021-01

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Abstract

Bacterial outer membrane vesicles (OMVs) perform a variety of functions in bacterial survival and virulence. In mammalian systems, OMVs activate immune responses and are exploited as vaccines. However, little work has focused on the interactions of OMVs with plant hosts. Here, we report that OMVs from Pseudomonas syringae and P. fluorescens activate plant immune responses that protect against bacterial and oomycete pathogens. OMV-mediated immunomodulatory activity from these species displayed different sensitivity to biochemical stressors, reflecting differences in OMV content. Importantly, OMV-mediated plant responses are distinct from those triggered by conserved bacterial epitopes or effector molecules alone. Our study shows that OMV-induced protective immune responses are independent of the T3SS and protein, but that OMV-mediated seedling growth inhibition largely depends on proteinaceous components. OMVs provide a unique opportunity to understand the interplay between virulence and host response strategies and add a new dimension to consider in host-microbe interactions.

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10.1016/j.celrep.2020.108645

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McMillan, Hannah M, Sophia G Zebell, Jean B Ristaino, Xinnian Dong and Meta J Kuehn (2021). Protective plant immune responses are elicited by bacterial outer membrane vesicles. Cell reports, 34(3). p. 108645. 10.1016/j.celrep.2020.108645 Retrieved from https://hdl.handle.net/10161/22486.

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Scholars@Duke

Hannah McMillan

Postdoctoral Associate
Dong

Xinnian Dong

Arts and Sciences Distinguished Professor of Biology

Using Arabidopsis thaliana as a model system, my laboratory studies the mechanisms of plant defense against microbial pathogens. We focus on a specific response known as systemic acquired resistance (SAR). SAR, which can be induced by a local infection, provides the plants with long lasting, systemic resistance against a broad spectrum of pathogens. Salicylic acid (SA; an active ingredient of aspirin) has been found to be the endogenous signal of SAR. Using a genetic approach, our laboratory identified genes involved in the regulation of SAR. Molecular and genetic analyses are being carried out to understand the gene function and to elucidate the SAR signaling pathway. These SAR-regulating genes are also favorite targets for molecular engineering of disease-resistance crops.

Kuehn

Margarethe Joanna Kuehn

Associate Professor of Biochemistry

Enterotoxigenic E. coli (ETEC) causes traveler's diarrhea and infant mortality in underdeveloped countries, and Pseudomonas aeruginosa is an opportunistic pathogen for immunocompromised patients. Like all gram negative bacteria studied to date, ETEC and P. aeruginosa produce small outer membrane vesicles that can serve as delivery "bombs" to host tissues. Vesicles contain a subset of outer membrane and soluble periplasmic proteins and lipids. In tissues and sera of infected hosts, vesicles have been observed to bud from the pathogen and come in close contact with epithelial cells. Despite their association with disease, the ability of pathogenic bacteria to distribute an arsenal of virulence factors to the host cells via vesicles remains relatively unexplored.

In our lab, we focus on the genetic, biochemical and functional features of bacterial vesicle production. Using a genetic screen, we have identified genes essential in the vesiculation process, we have identified specific proteins that are enriched in vesicles, and we have identified critical molecules that govern the internalization of vesicles into host cells. Using biochemical analysis of purified vesicles from cell-free culture supernatants, we have found that heat-labile enterotoxin, an important virulence factor of ETEC, is exported from the cells bound to the external surface of vesicles. Presented in this context, it is able to mediate the entry of the entire ETEC vesicle into human colorectal tissue culture cells. We have also discovered that the ability of vesicles to bind to specific cell types depends on their strain of origin: for example, P. aeruginosa vesicles produced by a strain that was cultured from the lungs of a patient with Cystic Fibrosis adhered better to lung than to gut epithelial cells, whereas a strain that was isolated from sera showed no such preference for lung cells. The vesicles stimulate epithelial cells and macrophages to elicit a cytokine response that is distinct from that of LPS (a major component of the vesicles) alone.

These studies will provide new insights into the membrane dynamics of gram-negative bacteria and consequently aid in the identification of new therapeutic targets for important human pathogens.


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