Bacterial metabolite sharing emerges from a balance between production and uptake

Microbial communities are structured by the exchange of metabolites. For example, vitamin B12 is used by many bacteria but produced by relatively few, meaning that exchange is likely important in natural settings. However, we do not understand how B12 is provisioned by those taxa that produce it. To uncover the mechanisms shaping extracellular metabolite pools, we quantified B12 synthesis, release, and uptake across hundreds of bacterial isolates from terrestrial and marine environments. In these data, four broad strategies emerged: Retainers (synthesis and high uptake), Providers (synthesis and low uptake), Scavengers (no synthesis, high uptake), and Bystanders (no synthesis and no uptake). For individual bacterial taxa, we found that extracellular B12 concentrations could be quantitatively predicted by considering vitamin release from lysis and reuptake by remaining living cells. Together, these results suggest that metabolite provisioning by bacteria may arise primarily via passive release through lysis and varying rates of reuptake by living cells. In this view, metabolite uptake by producers is a dominant force in controlling the size of external metabolite pools and thus their exchange.