Abstract
The study of chemical bioactivity in the rhizosphere has recently broadened to include microbial metabolites, and their roles in niche construction and competition via growth promotion, growth inhibition, and toxicity. Several prior studies have identified bacteria that produce volatile organic compounds (VOCs) with antifungal activities, indicating their potential use as biocontrol organisms to suppress phytopathogenic fungi and reduce agricultural losses. We sought to expand the roster of soil bacteria with known antifungal VOCs by testing bacterial isolates from wild and cultivated cranberry bog soils for VOCs that inhibit the growth of four common fungal and oomycete plant pathogens, and Trichoderma sp. Twenty one of the screened isolates inhibited the growth of at least one fungus by the production of VOCs, and isolates of Chromobacterium vaccinii had broad antifungal VOC activity, with growth inhibition over 90% for some fungi. Fungi exposed to C. vaccinii VOCs had extensive morphological abnormalities such as swollen hyphal cells, vacuolar depositions, and cell wall alterations. Quorum-insensitive cviR− mutants of C. vaccinii were significantly less fungistatic, indicating a role for quorum regulation in the production of antifungal VOCs. We collected and characterized VOCs from co-cultivation assays of Phoma sp. exposed to wild-type C. vaccinii MWU328, and its cviR− mutant using stir bar sorptive extraction and comprehensive two-dimensional gas chromatography—time-of-flight mass spectrometry (SBSE-GC × GC-TOFMS). We detected 53 VOCs that differ significantly in abundance between microbial cultures and media controls, including four candidate quorum-regulated fungistatic VOCs produced by C. vaccinii. Importantly, the metabolomes of the bacterial-fungal co-cultures were not the sum of the monoculture VOCs, an emergent property of their VOC-mediated interactions. These data suggest semiochemical feedback loops between microbes that have co-evolved for sensing and responding to exogenous VOCs.
Highlights
The health of any soil, and the productivity of the plants growing in it, is dependent on the activity and interactions of the microbes that are present (Berendsen et al, 2012; Xiong et al, 2017; Qiao et al, 2019)
These 21 isolates were analyzed for antifungal bacterial volatile organic compounds activity using a co-cultivation method that restricts microbial interactions to the gas phase
We quantified antifungal activity by measuring radial growth inhibition of bacterial volatile organic compounds (bVOCs)-exposed Trichoderma sp., Phoma sp., Colletotrichum sp., Coleophoma sp., and P. cinnamomi colonies compared to unexposed controls
Summary
The health of any soil, and the productivity of the plants growing in it, is dependent on the activity and interactions of the microbes that are present (Berendsen et al, 2012; Xiong et al, 2017; Qiao et al, 2019). There is a long history of observations indicating that plant and soil-associated bacteria produce inorganic and organic volatile compounds with antifungal activity (Dobbs and Hinson, 1953; Barr, 1976; Zygadlo et al, 1994; Zou et al, 2007; Effmert et al, 2012; Audrain et al, 2015; De Vrieze et al, 2015; Schmidt et al, 2016; Mülner et al, 2019), and that fungi produce antibacterial volatile organic compounds (VOCs) (Effmert et al, 2012; Werner et al, 2016). Over the past two decades, investigations into the production and biological activities of VOCs have resulted in a large catalog of compounds that are synthesized by soil microorganisms, often in intriguingly complex and dynamic combinations (Mackie and Wheatley, 1999; Fernando et al, 2005; Zou et al, 2007; Korpi et al, 2009; Insam and Seewald, 2010; Effmert et al, 2012; Penuelas and Terradas, 2014; Lemfack et al, 2017; Rajer et al, 2017; Schulz-Bohm et al, 2017; Yuan et al, 2017), though little is yet known about the semiochemical interactions that are mediated by VOCs, nor how those signals are transduced
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