Enhanced metabolic entanglement emerges during evolution of an interkingdom microbial community

The evolution of obligate symbioses from initially autonomous entities most likely occurred through a series of multiple intermediate steps, resulting in a gradual erosion of independence. Here we observed a progression towards such increased entanglement in an engineered mutualistic consortium between Escherichia coli and Saccharomyces cerevisiae. Experimental evolution of this interkingdom community led to a rapid enhancement of the metabolic cooperation between partners, including the reinforcement of both selfish and social traits, and the de-novo emergence of partial dependence of yeast on the bacterial partner for ammonium assimilation. Selection on social traits repeatedly occurred indirectly, via pleiotropies and trade-offs within cellular regulatory networks, and without mechanisms of partner choice. We propose that such indirect selection on traits may be a common mechanism in evolutionary transitions towards sociality.