Bacterial volatile organic compounds attenuate pathogen virulence via evolutionary trade-offs.
Journal
The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
02
08
2022
accepted:
04
01
2023
revised:
21
12
2022
pmc-release:
01
03
2024
pubmed:
13
1
2023
medline:
25
2
2023
entrez:
12
1
2023
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 36635489
doi: 10.1038/s41396-023-01356-6
pii: 10.1038/s41396-023-01356-6
pmc: PMC9938241
doi:
Substances chimiques
Volatile Organic Compounds
0
Soil
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
443-452Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/T010606/1
Pays : United Kingdom
Informations de copyright
© 2023. The Author(s), under exclusive licence to International Society for Microbial Ecology.
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