Abstract
Cross-feeding interactions, in which bacterial cells exchange costly metabolites to the benefit of both interacting partners, are very common in the microbial world. However, it generally remains unclear what maintains this type of interaction in the presence of non-cooperating types. We investigate this problem using synthetic cross-feeding interactions: by simply deleting two metabolic genes from the genome of Escherichia coli, we generated genotypes that require amino acids to grow and release other amino acids into the environment. Surprisingly, in a vast majority of cases, cocultures of two cross-feeding strains showed an increased Darwinian fitness (that is, rate of growth) relative to prototrophic wild type cells—even in direct competition. This unexpected growth advantage was due to a division of metabolic labour: the fitness cost of overproducing amino acids was less than the benefit of not having to produce others when they were provided by their partner. Moreover, frequency-dependent selection maintained cross-feeding consortia and limited exploitation by non-cooperating competitors. Together, our synthetic study approach reveals ecological principles that can help explain the widespread occurrence of obligate metabolic cross-feeding interactions in nature.
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Acknowledgements
We would like to thank W Boland and J Gershenzon for support and IT Baldwin, TF Cooper, K Hammerschmidt, M Kaltenpoth, E Kothe, E Libby, PB Rainey, W Ratcliff, S Schmidt, and two anonymous reviewers for helpful discussions and constructive criticism of the manuscript. This work was supported by the Jena School for Microbial Communication (C Kaleta, C Kost, SP, HM and SS), International Max Planck Research School (KB, C Kaleta, C Kost and SS), Volkswagen Foundation (C Kost), Max Planck Society (C Kost, MR), Fundacão Calouste Gulbenkian (LFdF), Fundacão para a Ciencia e a Tecnologia (LFdF), and Siemens SA Portugal (LFdF).
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Conceived the project: SP and C Kost. Designed the experiments: SP, C Kaleta and C Kost. Performed all experiments: SP. Developed the AA measurement protocol: HM and MR. Independently replicated some experiments (data not shown): HM. Performed AA measurements: HM, SP, and MR. Analysed the data: SP and C Kost. Developed and applied the CASOP-GS method: C Kaleta, KB, LFdF, and SS. Wrote the paper: SP and C Kost. Amended the manuscript: all authors.
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Pande, S., Merker, H., Bohl, K. et al. Fitness and stability of obligate cross-feeding interactions that emerge upon gene loss in bacteria. ISME J 8, 953–962 (2014). https://doi.org/10.1038/ismej.2013.211
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DOI: https://doi.org/10.1038/ismej.2013.211
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