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Evolution of genome fragility enables microbial division of labor.

Published version
Peer-reviewed

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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.

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Keywords

Streptomyces, division of labor, evolution, evolvability, multiscale modeling, Genome, Mutation, Genomics, Anti-Bacterial Agents

Journal Title

Mol Syst Biol

Conference Name

Journal ISSN

1744-4292
1744-4292

Volume Title

Publisher

Springer Science and Business Media LLC
Sponsorship
Gatsby Charitable Foundation (GATSBY) (G112566)
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO) (NWA StartImpuls, NWO/ENW‐VICI 865.17.004)