Ammonium is a central nutrient in aquatic systems. Yet, cell-specific ammonium assimilation among diverse functional plankton is poorly documented in field communities. Combining stable-isotope incubations (15N-ammonium, 15N2 and 13C-bicarbonate) with secondary-ion mass spectrometry, we quantified bulk ammonium dynamics, N2-fixation and carbon (C) fixation, as well as single-cell ammonium assimilation and C-fixation within plankton communities in nitrogen (N)-depleted surface waters during summer in the Baltic Sea. Ammonium production resulted from regenerated (≥91%) and new production (N2-fixation, ≤9%), supporting primary production by 78–97 and 2–16%, respectively. Ammonium was produced and consumed at balanced rates, and rapidly recycled within 1 h, as shown previously, facilitating an efficient ammonium transfer within plankton communities. N2-fixing cyanobacteria poorly assimilated ammonium, whereas heterotrophic bacteria and picocyanobacteria accounted for its highest consumption (~20 and ~20–40%, respectively). Surprisingly, ammonium assimilation and C-fixation were similarly fast for picocyanobacteria (non-N2-fixing Synechococcus) and large diatoms (Chaetoceros). Yet, the population biomass was high for Synechococcus but low for Chaetoceros. Hence, autotrophic picocyanobacteria and heterotrophic bacteria, with their high single-cell assimilation rates and dominating population biomass, competed for the same nutrient source and drove rapid ammonium dynamics in N-depleted marine waters.