Bacterial volatile organic compounds attenuate pathogen virulence via evolutionary trade-offs

Volatile organic compounds (VOCs) produced by soil bacteria have been shown to exert plant pathogen biocontrol potential owing to their strong antimicrobial activity. While the impact of VOCs on soil microbial ecology is well established, their effect on plant pathogen evolution is yet poorly unders...

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Bibliographic Details
Published in:The ISME Journal 2023-03, Vol.17 (3), p.443-452
Main Authors: Wang, Jianing, Raza, Waseem, Jiang, Gaofei, Yi, Zhang, Fields, Bryden, Greenrod, Samuel, Friman, Ville-Petri, Jousset, Alexandre, Shen, Qirong, Wei, Zhong
Format: Article
Language:English
Subjects:
Adaptation
Adaptation, Physiological
Antibiotics
Antigens
Antiinfectives and antibacterials
Antimicrobial activity
Antimicrobial agents
Bacillus
Bacteria
Biological control
Biosynthesis
Cross-tolerance
Ecological effects
Evolution
Genetic engineering
Immunological tolerance
Lipopolysaccharides
Membrane permeability
Microorganisms
Mutation
Organic compounds
Pathogenicity
Pathogens
Plant Diseases - microbiology
Ralstonia solanacearum - genetics
Soil
Soil bacteria
Soil microorganisms
Soil permeability
Soils
Tradeoffs
Virulence
Virulence - genetics
VOCs
Volatile organic compounds
Volatile Organic Compounds - pharmacology
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Summary:Volatile organic compounds (VOCs) produced by soil bacteria have been shown to exert plant pathogen biocontrol potential owing to their strong antimicrobial activity. While the impact of VOCs on soil microbial ecology is well established, their effect on plant pathogen evolution is yet poorly understood. Here we experimentally investigated how plant-pathogenic Ralstonia solanacearum bacterium adapts to VOC-mixture produced by a biocontrol Bacillus amyloliquefaciens T-5 bacterium and how these adaptations might affect its virulence. We found that VOC selection led to a clear increase in VOC-tolerance, which was accompanied with cross-tolerance to several antibiotics commonly produced by soil bacteria. The increasing VOC-tolerance led to trade-offs with R. solanacearum virulence, resulting in almost complete loss of pathogenicity in planta. At the genetic level, these phenotypic changes were associated with parallel mutations in genes encoding lipopolysaccharide O-antigen (wecA) and type-4 pilus biosynthesis (pilM), which both have been linked with outer membrane permeability to antimicrobials and plant pathogen virulence. Reverse genetic engineering revealed that both mutations were important, with pilM having a relatively larger negative effect on the virulence, while wecA having a relatively larger effect on increased antimicrobial tolerance. Together, our results suggest that microbial VOCs are important drivers of bacterial evolution and could potentially be used in biocontrol to select for less virulent pathogens via evolutionary trade-offs.
ISSN:1751-7362
1751-7370
DOI:10.1038/s41396-023-01356-6