Environmental stress leads to genome streamlining in a widely distributed species of soil bacteria

Bacteria have highly flexible pangenomes, which are thought to facilitate evolutionary responses to environmental change, but the impacts of environmental stress on pangenome evolution remain unclear. Using a landscape pangenomics approach, I demonstrate that environmental stress leads to consistent, continuous reduction in genome content along four environmental stress gradients (acidity, aridity, heat, salinity) in naturally occurring populations of Bradyrhizobium diazoefficiens (widespread soil-dwelling plant mutualists). Using gene-level network and duplication functional traits to predict accessory gene distributions across environments, genes predicted to be superfluous are more likely lost in high stress, while genes with multi-functional roles are more likely retained. Genes with higher probabilities of being lost with stress contain significantly higher proportions of codons under strong purifying and positive selection. Gene loss is widespread across the entire genome, with high gene-retention hotspots in close spatial proximity to core genes, suggesting Bradyrhizobium has evolved to cluster essential-function genes (accessory genes with multifunctional roles and core genes) in discrete genomic regions, which may stabilise viability during genomic decay. In conclusion, pangenome evolution through genome streamlining are important evolutionary responses to environmental change. This raises questions about impacts of genome streamlining on the adaptive capacity of bacterial populations facing rapid environmental change.