Mutualism breakdown underpins evolutionary rescue in an obligate cross-feeding bacterial consortium

Abstract Populations facing lethal environmental change can escape extinction through rapid genetic adaptation, a process known as evolutionary rescue. Despite extensive study, evolutionary rescue is largely unexplored in mutualistic communities, where it is likely constrained by the less adaptable partner. Here, we explored empirically the likelihood, population dynamics, and genetic mechanisms underpinning evolutionary rescue in an obligate mutualism involving cross-feeding of amino acids between auxotrophic Escherichia coli strains. We found that over 80% of populations overcame a severe decline when exposed to two distinct types of abrupt, lethal stress. Of note, in all cases only one of the strains survived by metabolically bypassing the auxotrophy. Crucially, the mutualistic consortium exhibited greater sensitivity to both stressors than a prototrophic control strain, such that reversion to autonomy was sufficient to alleviate stress below lethal levels. This sensitivity was common across other stresses, suggesting it may be a general feature of amino acid–dependent obligate mutualisms. Our results reveal that evolutionary rescue may depend critically on the specific genetic and physiological details of the interacting partners, adding rich layers of complexity to the endeavor of predicting the fate of microbial communities facing intense environmental deterioration.