Obligate Endosymbiosis Explains Genome Expansion During Eukaryogenesis

Abstract

The endosymbiosis of an alpha-proteobacterium that gave rise to mitochondria was one of the key events in eukaryogenesis. Common patterns in eukaryogenesis and present-day endosymbiotic relations include genomic streamlining of the symbiont, endosymbiotic gene transfer, and regulatory control by the host through protein targeting to the symbiont. One unique outcome for eukaryogenesis was a much more complex cell with a large genome, which may or may not be related to the mitochondrial endosymbiosis. Despite the existence of many plausible hypotheses for the observed patterns, a constructive evolutionary model in which these hypotheses can be studied is still lacking. Here we construct an evolutionary model of cell-cycle regulation to study how obligate endosymbiosis between two prokaryote-like cells impacts cellular behavior and genome evolution. The model does not predefine an explicit fitness criterion and thereby allows for the evolution of various emergent behaviors. For instance, even though we do not allow for communication between host and symbiont, they achieve implicit cell-cycle coordination through their interaction with the environment. This evolved cell-cycle coordination can drive genome expansion as well as symmetry breaking in genome size. Many replicate runs of our evolution experiment yield organisms with a large host and small symbiont genome, but interestingly, some yield the opposite. Still on long timescales, organisms with a large host and small symbiont genome perform best, and mimic the outcome of eukaryogenesis. By designing and studying a constructive evolutionary model of obligate endosymbiosis, we uncovered some of the forces that may drive the patterns observed in nature. Our results provide a theoretical foundation for patterns related to the mitochondrial endosymbiosis, such as genome size asymmetry, and reveal evolutionary outcomes that have not been considered so far, such as cell-cycle coordination without direct communication.