Nucleotide cross-feeding links the marine microbial carbon and nitrogen cycles

Metabolic cross-feeding between microbes shapes oceanic biogeochemical cycles, but is poorly understood. Using the abundant phytoplankter Prochlorococcus and sympatric heterotrophs as a model system, we present evidence of nucleotide cross-feeding within oceanic microbial ecosystems. We find that Prochlorococcus excretes significant levels of thymidine across a range of growth conditions and significant levels of purines under phosphorus-limited relative to phosphorus-replete conditions. We further find genomic evidence of niche partitioning among heterotrophs in their usage of nucleotides, with different groups specializing on either thymidine or purines, while some generalists use both. SAR11, the most abundant oceanic heterotroph, only has genes for using purines, with some sub-groups having genes for uptake only and others having additional genes for purine catabolism. Preliminary data suggests purine exposure lowers the growth rate of cells with uptake genes only. However, purine treated cultures also have enhanced DNA/cell, and after washing and resuspension in fresh media exhibit a much shorter lag phase, than untreated cells, suggesting an increased fraction of cells was poised to replicate. This raises the possibility that cells with uptake genes only may be able to use purines as an environmental signal that helps them synchronize to the daily metabolic rhythms of the ecosystem. Purine catabolism in turn releases carbon, reducing power and urea, but we find that most SAR11 cells with catabolism genes lack urease, suggesting they release urea back to the environment. Prochlorococcus is known to be a major urea scavenger, creating a putative cycle in which purines transfer carbon and reducing power from Prochlorococcus to SAR11 and urea returns nitrogen returns to Prochlorococcus. Finally, we find that the fraction of SAR11 cells with purine catabolism genes is highest in low-phosphorus regions of the oceans, similar to conditions under which we observed increased purine excretion in Prochlorococcus cultures. Our findings highlight how combining genomic and culture-based studies can reveal new links within the oceanic biogeochemical cycles, as well as the forces shaping them.