Pangenomes reveal genomic signatures of microbial adaptation to chronic soil warming

Evolutionary responses to anthropogenic climate change are irreversible and largely uncaptured by climate models. Below-ground carbon transformations represent an important natural mitigation solution, but novel adaptive traits may alter microbial climate feedback mechanisms. To better define microbial evolutionary responses to warming, we study microorganisms from an ongoing in situ soil warming experiment at the Harvard Forest Long-term Ecological Research (LTER) site where, for over three decades, soils are continuously heated 5 ºC above ambient temperatures. We hypothesize that across generations of chronic warming, genomic signatures within diverse bacterial lineages reflect adaptations related to growth and carbon utilization. From our culture collection of soil bacteria isolated from experimental heated and control plots, we sequenced genomes representing taxa dominant in soil communities and sensitive to warming, including independent lineages of Alphaproteobacteria, Actinobacteria, and Betaproteobacteria. We investigated differences in genomic attributes and patterns of functional gene content to identify genetic signatures of adaptation. Comparative pangenomics revealed differently abundant gene clusters with functional annotations related to carbon and nitrogen metabolism. We also observe differences in genome-wide codon usage bias between heated and control genomes, suggesting potential adaptive traits related to growth or growth efficiency. Together, these data illustrate the emergence of diverse lineage-specific adaptive traits as well as common ecological-evolutionary microbial responses to climate change.