Ralstonia solanacearum plant pathogenic bacterium can rapidly evolve more tolerant to volatile organic compounds produced by competitors

The soil microbes produce volatile organic compounds (VOCs) that can diffuse over long distances and have the ability to improve plant growth and suppress bacterial growth due to antimicrobial activity. While the impact of VOC on soil microbial ecology is well established, there are no studies exploring evolutionary consequences of VOC.

Here we investigated the phenotypic and genetic basis of plant pathogenic Ralstonia solanacearum adaptation to VOCs produced by Bacillus amyloliquefaciens T-5 soil bacterium for approximately 550 bacterial generations at low, intermediate and high VOC exposure levels. We found that VOC selection led to increase in VOC tolerance but reduction in pathogen growth and several virulence traits including motility, antioxidant activity, biofilm formation and extracellular polysaccharide production. VOC tolerance also correlated positively with tolerance to antibiotics commonly produced by soil bacteria, indicative of similar tolerance mechanism.

Crucially, evolving more tolerant to VOCs, led to loss of virulence in planta. At the genetic level, VOC tolerance was linked to parallel missense mutations in glycosyltransferase (wecA) and a small insertion in fimbrial type-4 assembly protein (pilM) in 12 out of 18 sequenced clones. Our results suggest that R. solanacearum can rapidly evolve more tolerant to VOCs produced by bacterial competitors.

However, this adaptation incurs significant fitness costs, leading to trade-offs with pathogen growth and virulence. Antimicrobial biocontrol strains could thus provide unexplored benefits by allowing steering of pathogen virulence via evolutionary trade-offs.

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