Abstract
The plant kingdom represents a prominent biodiversity island for microbes that associate with the below- or aboveground organs of vegetal species. Both the root and the leaf represent interfaces where dynamic biological interactions influence plant life. Beside well-studied communication strategies based on soluble compounds and protein effectors, bacteria were recently shown to interact both with host plants and other microbial species through the emissions of volatile organic compounds (VOCs). Focusing on the potato late blight-causing agent Phytophthora infestans, this work addresses the potential role of the bacterial volatilome in suppressing plant diseases. In a previous study, we isolated and identified a large collection of strains with anti-Phytophthora potential from both the phyllosphere and the rhizosphere of potato. Here we report the characterization and quantification of their emissions of biogenic volatiles, comparing 16 Pseudomonas strains differing in (i) origin of isolation (phyllosphere vs. rhizosphere), (ii) in vitro inhibition of P. infestans growth and sporulation behavior, and (iii) protective effects against late blight on potato leaf disks. We systematically tested the pharmacological inhibitory activity of core and strain-specific single compounds against P. infestans mycelial growth and sporangial behavior in order to identify key effective candidate molecules present in the complex natural VOCs blends. We envisage the plant bacterial microbiome as a reservoir for functional VOCs and establish the basis for finding the primary enzymatic toolset that enables the production of active components of the volatile bouquet in plant-associated bacteria. Comprehension of these functional interspecies interactions will open perspectives for the sustainable control of plant diseases in forthcoming agriculture.
Highlights
In order to correlate the production of specific bacterial VOCs (bVOCs) to the inhibitory potential of the 16 different Pseudomonas strains we previously screened, showing various volatile organic compounds (VOCs)-mediated inhibition against P. infestans (Hunziker et al, 2015), we trapped and identified the different chemical species they emitted
We chose to collect the bVOCs over a 24 h incubation period with the aim to maximize the chance of recovering chemoprofiles that would best represent the P. infestans growth-inhibiting bVOC blends occurring in our previously published dual-assays (Hunziker et al, 2015)
As for sporangia, the influence of pure compounds on the formation of germ tubes from encysted zoospores mostly resembled the effect on zoospore production. These results suggest that Pseudomonas bVOCs have the potential to alter and impede P. infestans development, and that bioactive compounds mostly act on the different lifeforms of the pathogen rather than interfering with only one or the other
Summary
After more than a decade of exploratory work, it is recognized that beside their well-documented, soluble antimicrobial arsenal, bacteria emit a wide range of volatile organic compounds (VOCs) that hold a strong inhibitory potential against microbial competitors (Garbeva et al, 2014; Audrain et al, 2015; Hunziker et al, 2015; Kanchiswamy et al, 2015; Schmidt et al, 2015). Bacterial VOCs (bVOCs) are currently bringing an additional motivation to prospect the plant-associated microbiome with respect to its ability to confer to crop plants a natural protection against microbial pathogens In natura, these molecules are suspected to mediate or participate in intra- and interspecies communication processes such as bacterial quorum sensing, growth, differentiation or antibiotic and stress resistance (Vespermann et al, 2007; Bailly and Weisskopf, 2012; Bos et al, 2013; Groenhagen et al, 2013; Audrain et al, 2015; Kanchiswamy et al, 2015). The pathosystem Phytophthora infestans-potato represents a good model to investigate VOCs’ contributions to the microbial relationships occurring at the plant soil and air interfaces This devastating pathogen, which causes the economically highly relevant potato late blight disease, can both infect aerial and soil organs. In addition to biogenic soluble chemicals or protein effectors, the quest for bacterial bio-control agents should take into account the enzymatic traits leading to the production of VOCs as they represent a supplementary defense line against infection by plant pathogens
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