Global niche partitioning of purine and pyrimidine cross-feeding among ocean microbes

Abstract

Characterizing the diversity of cross-feeding pathways in ocean microbes illuminates forces shaping co-evolution, ecosystem self-assembly and carbon cycling. Here we uncover a purine and pyrimidine cross-feeding network in globally abundant groups. The cyanobacterium Prochlorococcus exudes both compound classes, which metabolic reconstructions suggest follows synchronous daily genome replication. Co-occurring heterotrophs differentiate into purine or pyrimidine specialists, or generalists, and use compounds for different purposes. The most abundant heterotroph, SAR11, is a specialist that uses purines as sources of energy, carbon and/or nitrogen, with subgroups differentiating along ocean-scale gradients in the supply of energy and nitrogen, in turn leading to putative cryptic nitrogen cycles that link many microbes. Finally, in a SAR11 subgroup that dominates where Prochlorococcus is abundant, adenine additions to cultures inhibit DNA synthesis, poising cells for replication. We argue this subgroup uses inferred daily pulses of adenine from Prochlorococcus to metabolically synchronize to the daily supply of photosynthate from surrounding phytoplankton.