Trait-environmental relationships reveal microbial strategies of environmental adaptation

Microbial trait variation along environmental gradients is crucial to understanding their ecological adaptation mechanisms. With the increasing availability of microbial genomes, making full use of the genome-based traits to decipher their adaptation strategies becomes promising and urgent. Here, we examined microbial communities in water and sediments of 20 East African lakes with pH values ranging from 7.2 to 10.1 through taxonomic profiling and genome-centric metagenomics. We identified functional traits important for microbial adaptation to the stresses of alkalinity and salinity based on the significant trait-environment relationships (TERs), including those involved in cytoplasmic pH homeostasis, compatible solute accumulation, cell envelope modification, and energy requisition. By integrating these significant traits, we further developed an environmental adaptation index to quantify the species-level adaptive capacity for environmental stresses, such as high pH environments. The adaptation index of pH showed consistently significant positive relationships with species pH optima across regional and global genomic datasets from freshwater, marine, and soda lake ecosystems. The generality of the index for quantifying environmental adaptation was demonstrated by showing significant relationships with the species niche optima for the gradients of soil temperature and seawater salinity. These results highlight the importance of TERs in facilitating the inference of microbial genomic-based adaptation mechanisms and expand our understanding of ecological adaptive strategies along environmental gradients.