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

The full dataset used in this study is available on GitHub at https://github.com/ignamel/ER_mutualism.git and on Zenodo at https://doi.org/10.5281/zenodo.1499267063. All raw sequencing data is available on the US National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) under BioProject PRJNA1143481 (http://www.ncbi.nlm.nih.gov/bioproject/1143481). Source data are provided as a Source Data file. Source data are provided with this paper.

The Python 3.11.9 code used for analyzing, and creating figures is open-source and available on GitHub (https://github.com/ignamel/ER_mutualism.git) and stored at https://doi.org/10.5281/zenodo.1499267063.

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.

We thank Valeria Tsvichenko and Rotem Shner for the laboratory assistance, and members of the Friedman lab and Couce lab for helpful discussions. JF was supported by the Israel Science Foundation (grant No. 883/22). AC supported by the Agencia Estatal de Investigación (Centros de Excelencia “Severo Ochoa”, SEV-2016-0672 and CEX2020-000999-S; Proyectos de I+D+i, PID2022-142857NB-I00), and a Comunidad de Madrid “Talento” Fellowship (2019-T1/BIO−12882, 2023-5 A/BIO-28940). IJMJ was supported by “Margarita Salas” post-doctoral Fellowship (MS2021_003, Universidad de Málaga, Unión Europea–NextGeneration EU, Ministerio de Universidades, Spain).

With funding form the Spanish government through the "Severa Ochoa Centre of Excellence" accreditation (CEX2020-000999-S).

Peer reviewed