Evolution of genome fragility enables microbial division of labor

Author:

Colizzi Enrico Sandro123ORCID,van Dijk Bram4ORCID,Merks Roeland M H125ORCID,Rozen Daniel E5ORCID,Vroomans Renske M A236ORCID

Affiliation:

1. Mathematical Institute Leiden University Leiden The Netherlands

2. Origins Center Leiden The Netherlands

3. Sainsbury Laboratory Cambridge University Cambridge UK

4. Department of Microbial Population Biology Max Planck Institute for Evolutionary Biology Plön Germany

5. Institute of Biology Leiden University Leiden The Netherlands

6. Informatic Institute University of Amsterdam Amsterdam The Netherlands

Abstract

AbstractDivision 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.

Funder

Gatsby Charitable Foundation

Nederlandse Organisatie voor Wetenschappelijk Onderzoek

Publisher

Springer Science and Business Media LLC

Subject

Applied Mathematics,Computational Theory and Mathematics,General Agricultural and Biological Sciences,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,Information Systems

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