Date Published: June 1, 2017
Publisher: Public Library of Science
Author(s): Leron Katsir, Ofir Bahar, Cyril Zipfel.
Gram-negative bacteria outer membrane vesicles (OMVs) are extracellularly released blebs, constantly detaching from the bacterial cell surface. Being ubiquitous among bacteria and diverse in content, OMVs have a plethora of functions: promoting virulence, mediating bacterial cell–cell communication, modulating host immune response, and more. Though most research on OMVs has been carried out on animal pathogens, production of OMVs by plant pathogenic bacteria is predicted to be similarly intrinsic to their biology. Recent studies in the field of plant–bacteria interactions have begun to unravel the roles of OMVs, showing their involvement in biofilm formation, virulence, and modulation of plant immunity. With a range of general to highly specialized roles, these structures can act as an adaptive toolbox during pathogenesis and stress. This Pearl will crystallize current OMV research with a special focus on the role OMVs play in plant–bacteria interactions.
OMVs are formed continuously during growth and host colonization and are natural extensions of the bacteria producing them . The phospholipid membrane bilayer of OMVs also contains lipopolysaccharides (LPS) and outer membrane–localized proteins. The OMV lumen envelops periplasmic constituents such as peptidoglycans (PG), soluble proteins, and enzymes and can contain an array of other small molecules, including RNA and DNA.
Pathogen recognition is essential for the host to mount an effective immune response. Host cells may monitor for OMVs as a cue for pathogen invasion by recognizing OMV microbe-associated molecular patterns (MAMPs) . The perception of OMVs in mammalian systems is facilitated by cell surface and cytosolic receptor recognition of OMV MAMPs and was recently reviewed . Plants have only recently been shown to recognize and respond to OMVs purified from plant pathogens by activating typical innate immune responses . MAMP diversity in OMVs is large and ranges from integral elements like LPS and PG to variable proteinaceous cargo such as Elongation Factor-Tu (EF-Tu) and flagellin, which have been found to be associated with purified OMVs [3,4,10,13]. This complex array of immune elicitors can be recognized by plant immune receptors known as pattern recognition receptors (PRRs), which have extracellular domains for MAMP recognition (Fig 1) .
OMVs are beneficial to bacterial pathogens in the context of host colonization . In addition to mitigating the effects of host-produced antibiotics through increased vesiculation, OMVs can shield the bacterial body from antibiotics by carrying enzymes that mediate antibiotic protection . The packaging and delivery of key molecules and enzymes in and by OMVs have implications in regulating host development, biofilm formation, nutrient acquisition, and in promoting disease (Fig 1).
Clearly, understanding the biology of plant–bacteria interactions is not complete without accounting for OMVs. The multitude of roles played by these extracellular organelles, from immune modulation to regulation of biofilms, nutrient acquisition, protein secretion, and detoxification, makes them a multifunction tool, much like a Swiss Army knife, available to respond to a variety of challenges. Whether bacteria can in fact select the tool set or if the OMV is only a microcosm of what is synthesized in the bacterial body remains to be seen. The rich species diversity of plant pathogenic bacteria offers many avenues for investigation into the way bacteria utilize these tools in specific plant–bacteria interactions. Beyond plant pathogenic bacteria, other microorganisms such as plant pathogenic fungi, nematodes, and also mutualistic microorganisms like rhizobia are likely to secrete extracellular vesicles [25,26]. The role of these extracellular vesicles in pathogenesis and in symbiosis is a fascinating area of research. It is clear we have barely crossed the outer membrane of plant–bacteria OMV research.