The trade-off between individual metabolic specialization and versatility determines the metabolic efficiency of microbial communities

Abstract In microbial systems, a metabolic pathway can be either completed by one autonomous population or alternatively be distributed among a consortium performing metabolic division of labor (MDOL), where several specialized populations cooperate to complete the pathway. MDOL facilitates the system’s function by reducing the metabolic burden; however, it may also hinder the function by reducing the exchange efficiency of metabolic intermediates among individuals. As a result, the metabolic efficiency of a community is influenced by trade-offs between the metabolic specialization and versatility of individuals, with the latter potentially introducing metabolic redundancy into the community. However, it remains unclear how metabolic specialization and versatility of the individuals involved can be controlled in order to optimize the function of the community. In this study, we deconstructed the metabolic pathway of naphthalene degradation into four specialized steps and introduced them individually or combinatorically into different strains, with varying levels of metabolic specialization. Using these strains, we engineered 1,456 synthetic consortia with varying levels of metabolic redundancy and tested their naphthalene degradation efficiency. We found that 74 consortia possessing metabolic redundancy exhibited higher degradation efficiency than both the autonomous population and the rigorous MDOL community. Quantitative modeling derived from our experiments provides general strategies for identifying the most effective MDOL consortium with functional redundancy (MCFR) from a range of possible MCFRs. Our large-scale genomic analysis suggests that natural communities for hydrocarbon degradation are mostly functionally redundant. In summary, our study provides critical insights into the engineering of high-performance microbial systems and explains why functional redundancy is prevalent in natural microbial communities.