Title: | Bacterial volatile organic compounds attenuate pathogen virulence via evolutionary trade-offs |
Author(s): | Wang J; Raza W; Jiang G; Yi Z; Fields B; Greenrod S; Friman VP; Jousset A; Shen Q; Wei Z; |
Address: | "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. 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. waseem@njau.edu.cn. Institute for Environmental Biology, Ecology & Biodiversity, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands. waseem@njau.edu.cn. Department of Biology, University of York, Wentworth Way, York, YO10 5DD, UK. 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. ville-petri.friman@helsinki.fi. Department of Biology, University of York, Wentworth Way, York, YO10 5DD, UK. ville-petri.friman@helsinki.fi. Department of Microbiology, University of Helsinki, Helsinki, 00014, Finland. ville-petri.friman@helsinki.fi. 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. weizhong@njau.edu.cn" |
DOI: | 10.1038/s41396-023-01356-6 |
ISSN/ISBN: | 1751-7370 (Electronic) 1751-7362 (Print) 1751-7362 (Linking) |
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" |
Keywords: | "*Volatile Organic Compounds/pharmacology Virulence/genetics *Bacillus Adaptation, Physiological Soil *Ralstonia solanacearum/genetics Plant Diseases/microbiology;" |
Notes: | "MedlineWang, Jianing Raza, Waseem Jiang, Gaofei Yi, Zhang Fields, Bryden Greenrod, Samuel Friman, Ville-Petri Jousset, Alexandre Shen, Qirong Wei, Zhong eng BB/T010606/1/BB_/Biotechnology and Biological Sciences Research Council/United Kingdom Research Support, Non-U.S. Gov't England 2023/01/13 ISME J. 2023 Mar; 17(3):443-452. doi: 10.1038/s41396-023-01356-6. Epub 2023 Jan 12" |