DNA supercoiling (SC), the level of under-or overwinding of the DNA polymer around itself, is widely recognized as an ancestral regulation mechanism of gene expression in bacteria. Higher negative SC levels facilitate the opening of the DNA double helix at gene promoters, and increase the associated expression levels. Different levels of SC have been measured in bacteria exposed to different environments, leading to the hypothesis that SC variation can be an environmental response. Moreover, DNA transcription has been shown to generate local variations in the SC level, and therefore to impact the transcription of neighboring genes. In this work, we study the coupled dynamics of DNA supercoiling and transcription at the genome scale. We implement a genome-wide model of gene expression based on the transcription-supercoiling coupling (TSC). We show that, in this model, a simple change in global DNA SC is sufficient to trigger differentiated responses in gene expression levels via the TSC. Then, studying our model in the light of evolution, we demonstrate that this SC-mediated non-linear response to environmental change can serve as the basis for the evolution of specialized phenotypes, through the selection of a specific genomic architecture.