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ABSTRACT Prochlorococcusis an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade ofProchlorococcus, nearly all cells can assimilate nitrite (NO₂⁻), with a subset capable of assimilating nitrate (NO₃⁻). LLI cells are maximally abundant near the primary NO₂⁻maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO₃⁻reduction and subsequent NO₂⁻release by phytoplankton. We hypothesized that someProchlorococcusexhibit incomplete assimilatory NO₃⁻reduction and examined NO₂⁻accumulation in cultures of threeProchlorococcusstrains (MIT0915, MIT0917, and SB) and twoSynechococcusstrains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO₂⁻during growth on NO₃⁻. Approximately 20–30% of the NO₃⁻transported into the cell by MIT0917 was released as NO₂⁻, with the rest assimilated into biomass. We further observed that co-cultures using NO₃⁻as the sole N source could be established for MIT0917 andProchlorococcusstrain MIT1214 that can assimilate NO₂⁻but not NO₃⁻. In these co-cultures, the NO₂⁻released by MIT0917 is efficiently consumed by its partner strain, MIT1214. Our findings highlight the potential for emergent metabolic partnerships that are mediated by the production and consumption of N cycle intermediates withinProchlorococcuspopulations. IMPORTANCEEarth’s biogeochemical cycles are substantially driven by microorganisms and their interactions. Given that N often limits marine photosynthesis, we investigated the potential for N cross-feeding within populations ofProchlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, someProchlorococcuscells release extracellular NO₂⁻during growth on NO₃⁻. In the wild,Prochlorococcuspopulations are composed of multiple functional types, including those that cannot use NO₃⁻but can still assimilate NO₂⁻. We show that metabolic dependencies arise whenProchlorococcusstrains with complementary NO₂⁻production and consumption phenotypes are grown together on NO₃⁻. These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates.