Plant growth-promoting rhizobacteria benefit plants by stimulating their growth or protecting them against phytopathogens. Rhizobacteria must colonize and persist on plant roots to exert their benefits. However, little is known regarding the processes by which rhizobacteria adapt to different plant species, or behave under alternating host plant regimes. Here, we used experimental evolution and whole-population whole-genome sequencing to analyse how Bacillus subtilis evolves on Arabidopsis thaliana and tomato seedlings, and under an alternating host plant regime, in a static hydroponic setup. We observed parallel evolution across multiple levels of biological organization in all conditions, which was greatest for the two heterogeneous, multi-resource, spatially structured environments at the genetic level. Species-specific adaptation at the genetic level was also observed, possibly caused by the selection stress imposed by different host plants. Furthermore, a trade-off between motility and biofilm development was supported by mutational changes in motility- and biofilm-related genes. Finally, we identified several condition-specific and common targeted genes in different environments by comparing three different B. subtilis biofilm adaptation settings. The results demonstrate a common evolutionary pattern when B. subtilis is adapting to the plant rhizosphere in similar conditions, and reveal differences in genetic mechanisms between different host plants. These findings will likely support strain improvements for sustainable agriculture.
Laboratory experimental evolution provides a powerful tool for studying microbial adaptation to different environments. To understand the differences and similarities of the dynamic evolutionary landscapes of two model species from the Bacillus genus as they adapt to abiotic and biotic surfaces, we revived the archived population samples from our four previous experimental evolution studies and performed longitudinal whole-population genome sequencing. Surprisingly, higher number of mutations, higher genotypic diversity, and higher evolvability were detected in the biotic conditions with smaller population size. Different adaptation strategies were observed in different environments within each species, with more diversified mutational spectrum detected in biotic conditions. The insertion sequences of Bacillus thuringiensis are critical for its adaptation to the plastic bead-attached biofilm environment, but insertion sequence mobility was a general phenomenon in this species independent of the selection condition. Additionally, certain parallel evolution has been observed across species and environments, particularly when two species adapt to the same environment at the same time. Further, the higher degree of genetic diversification observed in biotic selective environments indicates an increased spatial niche heterogeneity and a nutritional source difference created by the plant host that provided a strong strength of selection during the adaptation process. Together, these results provide the first comprehensive mutational landscape of two bacterial species biofilms that is adapted to an abiotic and biotic surface.
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