TY - JOUR
T1 - Inhibition of Fungal Growth and Induction of a Novel Volatilome in Response to Chromobacterium vaccinii Volatile Organic Compounds
AU - Ebadzadsahrai, Ghazal
AU - Higgins Keppler, Emily A.
AU - Soby, Scott D.
AU - Bean, Heather D.
N1 - Funding Information:
P. chlororaphis 30-84 was generously provided by Leland (Sandy) Pierson at Texas A&M, Phytophthora cinnamomi R001 was generously provided by Jerry Weiland at Oregon State University/USDA/ARS. Trenton Davis provided statistical assistance for the analysis of GC × GC-TOFMS data. Alisha Harrison conducted HCN assays and provided technical assistance on maintenance, identification, and sequencing of microbial isolates. The authors would like to especially thank David Lowry, Arizona State University for TEM images. Funding. Support for the project came from Midwestern University and Arizona State University internal funds. Open access publication fees came from the Biomedical Sciences Program at Midwestern University.
Publisher Copyright:
© Copyright © 2020 Ebadzadsahrai, Higgins Keppler, Soby and Bean.
PY - 2020/5/20
Y1 - 2020/5/20
N2 - 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.
AB - 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.
KW - emergent properties
KW - fungal pathogen antagonism
KW - inter-kingdom communication
KW - quorum sensing (QS)
KW - semiochemical communication
KW - volatile organic compound (VOC)
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UR - http://www.scopus.com/inward/citedby.url?scp=85085876356&partnerID=8YFLogxK
U2 - 10.3389/fmicb.2020.01035
DO - 10.3389/fmicb.2020.01035
M3 - Article
AN - SCOPUS:85085876356
SN - 1664-302X
VL - 11
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
M1 - 1035
ER -