It is now well established that microbial community patterns reflect the importance of environmental conditions in governing the taxonomic and functional composition in various microbiomes. These observed community responses are largely associated with ecological processes; however, the evolutionary potential for microbes to adapt to environmental change remains largely unexplored in natural environments. While laboratory studies have repeatedly shown rapid evolutionary adaptation, it is unclear how in vitro observations of adaptive dynamics extend to natural communities and contribute to shifts in standing genetic variation (i.e., species composition).
To understand the degree to which ecological and evolutionary processes influence compositional response to environmental change, we conducted a large-scale reciprocal transplant study over 18 months across an elevation gradient in Southern California. Specifically, we performed two concurrent transplant experiments of 1) entire microbial communities, and 2) an isogenic strain belonging to the abundant bacterium, Curtobacterium. In both cases, we utilized a microbial cage system (to prevent dispersal) to transplant leaf litter communities or the isogenic strain onto sterile leaf litter to five sites covarying in temperature and precipitation.
Results/Conclusions
Previously we demonstrated that the transplanted communities (as assessed by 16S rRNA amplicons) shifted to reflect the abiotic environment regardless of initial community inoculum. To assess evolutionary responses (genetic changes in a population), here we first utilized 120 metagenomic samples to provide finer genetic resolution to track shifts in ecological populations (ecotypes) of Curtobacterium. Similar to the community patterns, we found site effects explained 28.5% of the variation in ecotype composition (p < 0.001). In particular, ecotype IB/C strongly drove compositional differences when transplanted to the hotter, drier sites. Thus, the observed shifts in the standing genetic variation of Curtobacterium ecotypes suggest that both ecological and evolutionary processes are contributing to environmental responses.
While local adaptation may be ongoing, the adaptive changes within a species can be difficult to detect compared to community level shifts. Therefore, in a second experiment, we tracked evolutionary changes of a single, isogenic strain across the same environmental gradient. Using a combination of genomics and metagenomics, we identified a variety of genomic mutations over the 18-month period associated with various sites, including metal resistance proteins and RNA polymerase subunits. Ultimately, both field experiments demonstrated the potential for rapid evolutionary change (within 18 months) by a soil bacterium in response to natural environmental variation.