The population dynamics in the coastal bacterioplankton community off Plymouth (UK) was studied in samples proportionally diluted (99%, 90%, 66% and 0%) with sterile seawater, incubated in the dark for 2–4 days and monitored by flow cytometry. Nucleic acid content of cells, stained with SYBR Green I DNA specific dye, was used as an index of a genome size. Using flow sorting and fluorescence in situ hybridization (FISH) with a set of ribosomal RNA targeted oligonucleotide probes, the phylogenetic composition of dominant cytometric groups of bacterioplankton was determined to be similar during growth in the dilution series. The proportion of the low nucleic acid (LNA) group decreased and correspondingly the high nucleic acid (HNA) groups increased with dilution. The assimilation rates of free amino acids, a highly labile nutrient pool, were determined by flow sorting the dominant groups after short incubations with 35S-methionine tracer. The relative cellular amino acid assimilation by the LNA cells increased with dilution, while the activity of the HNA cells either decreased or remained unchanged. However, highly metabolically active LNA bacteria were overgrown by the HNA bacteria, presumably because the small genome size—an adaptation to living in an oligotrophic environment—did not allow the LNA group to grow sufficiently fast to compete with the HNA group under experimentally reduced grazing pressure. To examine the experimental results a numerical model of bacterioplankton population dynamics was formulated based on the hypothesis that the LNA cells consume only a labile fraction of organic nutrients (amino acids etc.), while the HNA cells feed on both the labile and more refractory sources of nutrients, and that in the absence of phytoplankton the labile source of nutrients is produced entirely by the bacterivorous flagellates. The model simulations gave credence to the hypothesized primary dependence of the LNA group on labile organic nutrients recycled within the microbial loop.