In the North Atlantic Ocean, we found that natural populations of Prochlorococcus adhered to Redfield ratio dimensions when comparing cell quotas of carbon to nitrogen, but had flexible composition under nutrient and light stress, allowing for a broad range of cellular carbon- and nitrogen-to-phosphorus ratios. Synechococcus populations also exhibited a wide range of elemental stoichiometry, including carbon-to-nitrogen ratios and increased their carbon-to-phosphorus ratios in response to low dissolved phosphorus availability. Small eukaryotic populations tended to have lower carbon-to-phosphorus ratios than single cell cyanobacterial groups, with the exception of one group of samples, which highlights the importance of community composition when determining how biological diversity influences bulk particle stoichiometry. The ratio of dissolved nitrogen:phosphorus fluxes into the euphotic zone was not correlated to nitrogen:phosphorus cellular quotas. The lack of a homeostatic relationship implies that other mechanisms, such as species-specific adaptation to oligotrophic phosphorus concentrations, control elemental particle ratios.