Production and cross-feeding of nitrite within Prochlorococcus populations

ABSTRACT Prochlorococcus is an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade of Prochlorococcus, 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 some Prochlorococcus exhibit incomplete assimilatory NO3− reduction and examined NO2− accumulation in cultures of three Prochlorococcus strains (MIT0915, MIT0917, and SB) and two Synechococcus strains (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 and Prochlorococcus strain 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 within Prochlorococcus populations. IMPORTANCE Earth’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 of Prochlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, some Prochlorococcus cells release extracellular NO2− during growth on NO3−. In the wild, Prochlorococcus populations are composed of multiple functional types, including those that cannot use NO3− but can still assimilate NO2−. We show that metabolic dependencies arise when Prochlorococcus strains 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. Earth’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 of Prochlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, some Prochlorococcus cells release extracellular NO2− during growth on NO3−. In the wild, Prochlorococcus populations are composed of multiple functional types, including those that cannot use NO3− but can still assimilate NO2−. We show that metabolic dependencies arise when Prochlorococcus strains 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.