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

Abstract

Cross-feeding involves microbes consuming exudates of other surrounding microbes, mediating elemental cycling. Characterizing the diversity of cross-feeding pathways in ocean microbes illuminates evolutionary forces driving self-organization of ocean ecosystems. Here, we uncover a purine and pyrimidine cross-feeding network in globally abundant groups. The cyanobacterium <i>Prochlorococcus</i> exudes both compound classes, which metabolic reconstructions suggest follows synchronous daily genome replication. Co-occurring heterotrophs differentiate into purine- and pyrimidine-using generalists or specialists that 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 producing putative cryptic nitrogen cycles that link many microbes. Last, in an SAR11 subgroup that dominates where <i>Prochlorococcus</i> is abundant, adenine additions to cultures inhibit DNA synthesis, poising cells for replication. We argue that this subgroup uses inferred daily adenine pulses from <i>Prochlorococcus</i> to synchronize to the daily photosynthate supply from surrounding phytoplankton.