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

The ISME Journal volume 17, pages 443–452 (2023)Cite this article

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Abstract

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.

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Fig. 1: Schematic representation of the experimental design, where plant pathogenic Ralstonia solanacearum was evolved in the absence and presence of three VOC mixture concentrations in sealed flasks for 22 days with two-day serial transfers.
Fig. 2: Population density dynamics of plant pathogenic Ralstonia solanacearum in the absence and presence of three concentrations of volatile organic compound (VOC) mixture.
Fig. 3: Selection by volatile organic compounds (VOCs) leads to increased tolerance to both VOCs and antibiotics.
Fig. 4: Evolution of volatile organic compound (VOC)-tolerance leads to trade-off with Ralstonia solanacearum virulence.
Fig. 5: Evolution of volatile organic compounds (VOC)-tolerance leads to trade-off with Ralstonia solanacearum virulence.
Fig. 6: Volatile organic compounds (VOC)-tolerance is linked to parallel mutations in lipopolysaccharide and type-IV pilus encoding genes.
Fig. 7: Comparison of tolerance of evolved clones and ΔpilMiG and ΔwecAiC mutants to volatile organic compounds (VOC) and antibiotics.
Fig. 8: Comparison of virulence traits in vitro and in planta (disease index) of evolved clones and ΔpilMiG and ΔwecAiC mutants.

Data availability

The genome sequences of ancestral, No-VOC and H-VOC clones of Ralstonia solanacearum QL-Rs1115 are available at NCBI Sequence Read Archive (SRA) under the accession number SAMN29421919. The rest of the data are available in the article and its online supplementary material.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 42090064, 42090062, 42007038, 31972504, 32170180, 42277113, 41922053) to ZW, GJ and QS, and the National Key Research and Development Program of China (No. 2018YFD1000800), the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement (No. 838710-ReproDev to WR), the Royal Society (No. RSG\R1\180213 and No. CHL\R1\180031 to VPF) and jointly by a grant from UKRI, Defra, and the Scottish Government, under the Strategic Priorities Fund Plant Bacterial Diseases Programme (No. BB/T010606/1 to VPF), the Natural Science Foundation of Jiangsu Province (No. BK20190518), the Fundamental Research Funds for the Central Universities (grant no. XUEKEN2022025), and the Jiangxi Branch of China National Tobacco Corporation, China (grant no. 2021.01.010).

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Author notes

  1. These authors contributed equally: Jianing Wang, Waseem Raza, Gaofei Jiang.

Authors and Affiliations

  1. Jiangsu Provincial Key Lab for Organic Solid Waste Utilization, National Engineering Research Center for Organic-based Fertilizers, Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, Nanjing Agricultural University, Weigang 1, Nanjing, 210095, PR China

    Jianing Wang, Waseem Raza, Gaofei Jiang, Zhang Yi, Ville-Petri Friman, Alexandre Jousset, Qirong Shen & Zhong Wei

  2. Institute for Environmental Biology, Ecology & Biodiversity, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands

    Waseem Raza

  3. Department of Biology, University of York, Wentworth Way, York, YO10 5DD, UK

    Bryden Fields, Samuel Greenrod & Ville-Petri Friman

  4. Department of Microbiology, University of Helsinki, Helsinki, 00014, Finland

    Ville-Petri Friman

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  1. Jianing Wang
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Contributions

WR, ZW, AJ, VPF and SQ conceived the study and designed the experiments; WR, ZY and JW performed the evolution experiment and in vitro and in planta assays; BF and SG performed the variant calling analysis; GJ, ZY and JW performed the reverse-genetics experiment; WR, GJ, BF and VPF wrote the manuscript with input from all authors.

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Correspondence to Waseem Raza, Ville-Petri Friman or Zhong Wei.

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Wang, J., Raza, W., Jiang, G. et al. Bacterial volatile organic compounds attenuate pathogen virulence via evolutionary trade-offs. ISME J 17, 443–452 (2023). https://doi.org/10.1038/s41396-023-01356-6

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