Initial community composition determines the long-term dynamics of a microbial cross-feeding interaction

Multi-step substrate consumption pathways are ubiquitous and can promote biodiversity within microbial communities. If one cell-type preferentially consumes a primary substrate over the subsequently formed intermediates, then other cell-types specializing at consuming the intermediates can proliferate and engage in a cross-feeding interaction. Under what conditions will the interaction (and thus biodiversity) persist or disappear over time? To address this, we propagated communities consisting of two Pseudomonas stutzeri strains. One completely reduces nitrate to nitrogen gas but preferentially reduces nitrate over nitrite (referred to as the generalist), while the other cannot reduce nitrate and only reduces nitrite to nitrogen gas (referred to as the specialist). We found that the initial ratio of specialist-to-generalist (rS/G) determines the long-term dynamics and phenotypic trajectory of the cross-feeding interaction. The cause of these different dynamics is that the initial rS/G determines the initial environment and phenotypes acquired by the generalist, where lower initial rS/Gs create environments selecting for phenotypes with improved nitrite reduction. Our results demonstrate that initial community composition determines the phenotypic trajectory and fate of a cross-feeding interaction, and is therefore an important design consideration when engineering synthetic microbial communities.