Carbon limitation drives GC content evolution of a marine bacterium in an individual-based genome-scale model.

Abstract

An important unanswered question in evolutionary genomics is the source of considerable variation of genomic base composition (GC content) even among organisms that share one habitat. Evolution toward GC-poor genomes has been considered a major adaptive pathway in the oligotrophic ocean, but GC-rich bacteria are also prevalent and highly successful in this environment. We quantify the contribution of multiple factors to the change of genomic GC content of Ruegeria pomeroyi DSS-3, a representative and GC-rich member in the globally abundant Roseobacter clade, using an agent-based model. The model simulates 2 × 108 cells, which allows random genetic drift to act in a realistic manner. Each cell has a whole genome subject to base-substitution mutation and recombination, which affect the carbon and nitrogen requirements of DNA and protein pools. Nonsynonymous changes can be functionally deleterious. Together, these factors affect the growth and fitness. Simulations show that experimentally determined mutation bias toward GC is not sufficient to build the GC-rich genome of DSS-3. While nitrogen availability has been repeatedly hypothesized to drive the evolution of GC content in marine bacterioplankton, our model instead predicts that DSS-3 and its ancestors have been evolving in environments primarily limited by carbon.