Temperate coastal marine habitats are replete with complex biotic and abiotic interactions that mediate relationships and niche space between resident microbial community members. The dynamics of these interactions are amplified during spring and summer when phytoplankton form massive blooms and heterotrophic bacterioplankton respond to the successional release of high molecular weight dissolved organic matter (DOM, e.g., proteins, polysaccharides, lipids) as algal cells lyse. Dedicated clades of copiotrophic bacterioplankton adapted to high nutrient loads employ a suite of specialized enzymes and transporters for the degradation and uptake of large complex molecules like polysaccharides. Functional profiles of these carbohydrate active enzymes (CAZymes) reveal successions of niche spaces determined through substrate availability during bloom periods. As bacterioplankton process these substrates, algal-derived DOM is effectively incorporated into bacterioplankton biomass where it can be re-assimilated by higher protozoans and thus recycled within the food web or rapidly exported to sediments below. The net result is an enhancement of system-level efficiency and carbon export, respectively. In order to parse potential niche space in such a dynamic system, we first present diversity data derived from high-resolution temporal sampling (weekly to bi-weekly intervals) using the high-resolution oligotyping method Minimum Entropy Decomposition (MED) to cluster OTUs from 3 replicated sampling years 2010-2012. Differential abundance of MED OTUs >99% similar reveals a granularity of potential niche resolution that would not have been retrieved by traditional OTU clustering. Implementation of MED effectively extracts only those polymorphisms most relevant to in situ environmental selection pressure, essentially providing an ecological fingerprint of resident North Sea bacterioplankton. Despite inter-annual variation in phytoplankton blooms, we see a population of recurrent heterotrophic bacterioplankton during both baseline and bloom periods that is remarkably constrained in composition, relative community abundance and time of appearance each year for both abundant and rare OTUs. These robustly recurrent patterns reflect the selective power of seasonal forcing in shaping temperate microbial communities with low-frequency temperature-driven seasonal shifts. Superimposing effects of temperature are higher frequency shifts in OTUs during dynamic bloom events when substrate-induced forcing drives copiotrophic bacterioplankton communities, particularly within the Gammaproteobacteria and Flavobacteriia. Metagenome data from monthly sampling during spring blooms from these same years supports 16S rRNA diversity analyses revealing recurrent groups of specialized bloom taxa with highly constrained repertories of CAZymes. We demonstrate that even though there is substantial inter-annual variation of phytoplankton bloom intensity and taxonomic composition, the accompanying succession of bacterial clades is not a purely stochastic process, but also governed by deterministic principles such as temperature and substrate-induced forcing. The result is a resident bacterioplankton community containing as few as 6-14 dominant taxa each spring responsible for a vast majority of the diversity and thus potential function in a system previously thought to be considerably more stochastic and complex.