A major goal of marine microbial ecology is to understand how the environment structures microbiomes, and how community functions impact ocean biogeochemistry. Direct measurements of protein profiles through time reflect physiological functions of microbiomes and their adaptations to, and modifications of, local chemical gradients. We examined metaproteomes from two Arctic microbiomes during shipboard incubations to track early functional and taxonomic responses to simulated algal blooms and an oligotrophic control. Using a novel peptide-based enrichment analysis, significant changes (p-value < 0.01) in biological and molecular functions associated with carbon and nitrogen recycling were observed. Within the first day under both organic matter conditions, Bering Strait surface microbiomes increased protein synthesis, carbohydrate degradation and cellular redox processes while decreasing C1 metabolism. Taxonomic assignments revealed that the core microbiome collectively responded to algal substrates by synthesizing carbon prior to select taxa utilizing and reallocating nitrogen intracellularly. Incubations of Chukchi Sea bottom-water microbiomes showed similar, but temporally delayed, functional responses to identical conditions. This unbiased analysis of the dynamic responses of two oceanic microbiomes has important implications for timing and magnitude of bacterial responses to organic perturbations within the Arctic Ocean, and demonstrates how community-level functions could contribute to predicting biogeochemical gradients in oceans.