Evolution of genome fragility enables microbial division of labor

Abstract

Division of labor can evolve when social groups benefit from the functional specialization of its members. Recently, a novel means of coordinating the division of labor was found in the antibiotic‐producing bacterium Streptomyces coelicolor, where specialized cells are generated through large‐scale genomic re‐organization. We investigate how the evolution of a genome architecture enables such mutation‐driven division of labor, using a multiscale computational model of bacterial evolution. In this model, bacterial behavior—antibiotic production or replication—is determined by the structure and composition of their genome, which encodes antibiotics, growth‐promoting genes, and fragile genomic loci that can induce chromosomal deletions. We find that a genomic organization evolves, which partitions growth‐promoting genes and antibiotic‐coding genes into distinct parts of the genome, separated by fragile genomic loci. Mutations caused by these fragile sites mostly delete growth‐promoting genes, generating sterile, and antibiotic‐producing mutants from weakly‐producing progenitors, in agreement with experimental observations. This division of labor enhances the competition between colonies by promoting antibiotic diversity. These results show that genomic organization can co‐evolve with genomic instabilities to enable reproductive division of labor.