Reversion to metabolic autonomy underpins evolutionary rescue of a bacterial obligate mutualism

Abstract

Populations facing lethal environmental change can avoid extinction by undergoing rapid genetic adaptation, a phenomenon termed evolutionary rescue. While this phenomenon has been the focus of much theoretical and empirical research, our understanding of evolutionary rescue in communities consisting of interacting species is still limited, especially in mutualistic communities, where evolutionary rescue is expected to be constrained by the less adaptable partner. Here, we explored empirically the likelihood, population dynamics, and genetic mechanisms underpinning evolutionary rescue in an obligate mutualism in which auxotrophic Escherichia coli strains exchanged essential amino acids reciprocally. We observed that >80% of the communities avoided extinction when exposed to two different types of lethal and abrupt stresses. Of note, only one of the strains survived in all cases. Genetic and phenotypic analyses show that this strain reverted to autonomy by metabolically bypassing the auxotrophy, but we found little evidence of specific adaptation to the stressors. Crucially, we found that the mutualistic partners were substantially more sensitive to both stresses than prototrophs, so that reversion to autonomy was sufficient to alleviate stress below lethal levels. We observed that increased sensitivity was common across several other stresses, suggesting that this may be a general property of obligate mutualisms mediated by amino acid exchange. 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.