Rapid evolution of bacterial mutualism in the plant rhizosphere

Abstract

SummaryEven though beneficial plant-microbe interactions are commonly observed in nature, direct evidence for the evolution of bacterial mutualism in the rhizosphere remains elusive. Here we use experimental evolution to causally show that initially plant-antagonistic Pseudomonas protegens bacterium evolves into mutualists in the rhizosphere of Arabidopsis thaliana within six plant growth cycles (6 months). This evolutionary transition was accompanied with increased mutualist fitness via two mechanisms: i) improved competitiveness for root exudates and ii) enhanced capacity for activating the root-specific transcription factor gene MYB72, which triggers the production of plant-secreted scopoletin antimicrobial for which the mutualists evolved relatively higher tolerance to. Genetically, mutualism was predominantly associated with different mutations in the GacS/GacA two-component regulator system, which conferred high fitness benefits only in the presence of plants. Together, our results show that bacteria can rapidly evolve along the parasitism-mutualism continuum in the plant rhizosphere at an agriculturally relevant evolutionary timescale.

Experimental evolution ofBacillus subtilisonArabidopsis thalianaroots reveals fast adaptation and improved root colonization in the presence of soil microbes

“…Several studies have reported experimental evolution as a powerful tool to explore how bacteria adapt to ecologically relevant environments. A recent study investigated the adaptive response of the PGPR Pseudomonas protegens to the A. thaliana rhizosphere in a sand system, which revealed mutations in genes encoding global regulators and genes related to motility and cell surface structure across independent populations [61] and during such adaptation, the initially plant-antagonistic P. protegens bacterium evolved into mutualists [44]. Furthermore, Lin et al (2020) observed that adaptation of Bacillus thuringiensis to A. thaliana roots under hydroponic conditions led to the evolution of multicellular aggregating phenotypes, which, surprisingly, in certain lineages were accompanied by enhanced virulence against the Galleria mellonella larvae.…”

“…For these experiments, the resulting normalized values were subjected to a One-sample t-test to test whether the mean was significantly different from 1. For pairwise competitions between the ancestor and evolved isolates on the root or in LB + xylan, the relative fitness (r) of the evolved isolate was calculated by comparing the frequency of the evolved isolate at the beginning and the end of the competition experiment as shown in equation 1 [42][43][44], in which X0 is the initial and X1 is the final frequency of the evolved isolate. The relative fitness was log2-transformed, and these values were subjected to a One-sample t-test to test whether the mean was significantly different from 0.…”

Plant pathogenic bacterium can rapidly evolve tolerance to an antimicrobial plant allelochemical

“…Antimicrobial tolerance is also important for plant-bacteria interactions, as it can help bacteria to tolerate antimicrobials secreted by plants, such as coumarins, giving them a selective advantage in the plant rhizosphere microbiome (Stringlis et al, 2018). Such tolerance has recently been shown to evolve de novo in Pseudomonas protegens CHA0 bacterium against the antimicrobial scopoletin secreted by Arabidopsis thaliana (Li et al, 2021). Prolonged exposure to plant allelochemicals could thus select for more tolerant plant pathogen genotypes also during biofumigation and will likely be affected by the strength and duration of ITC exposure, which is important in determining whether potential tolerance or resistance mutations have enough time to sweep through pathogen populations.…”