The dissolved organic matter (DOM) released by living marine phytoplankton cells supports communities of associated bacteria that are predictably dominated by members of the Rhodobacterales, Flavobacteriales, and families within the Gammaproteobacteria. These bacteria rapidly assimilate phytoplankton exometabolites within hours to days of release. Little is known about the chemical composition of this pool of labile DOM, however, which is difficult to characterize through current chemical methods. This dissertation addresses two main questions: 1) What metabolites mediate organic matter flux between phytoplankton and bacteria in the surface ocean? And 2) How is metabolite use partitioned among the different bacterial taxa that associate with phytoplankton cells? To address these, two different approaches were used. In Chapters 2 and 3, co-culture systems were established with model marine phytoplankton and bacteria, utilizing the bacteria as biosensors to recognize phytoplankton exometabolites. In Chapter 4, temporal dynamics of bacterial transporters during a natural phytoplankton bloom were used to infer substrate utilization capabilities of environmental bacteria represented by Metagenome Assembled Genomes (MAGs). In both Chapters 2 and 3, I found that overlap in bacterial use of phytoplankton-derived metabolites was low, suggesting resource niche partitioning between bacterial taxa. A comparison of the hypothesized Micromonas metabolite pool with that of Thalassiosira indicated that, for both phytoplankton, heterotrophic bacteria transcription signaled recognition of fatty acids, nucleosides, and amino acids. Key differences were a greater polysaccharide uptake signal when bacteria were dependent on Thalassiosira for substrates compared to Micromonas, and the specific organic nitrogen and sulfur transporters each induced in the bacteria. In Chapter 4, the MAG genome content and temporal dynamics provided a window into the substrate acquisition capabilities of the heterotrophic bacterial members in the bloom. Transporter annotations were used to hypothesize the target substrates being assimilated by the ten most abundant MAGs. Studying the capabilities and dynamics of the dominant bacteria through the progression of a coastal bloom provided a perspective on the substrate niche space of the heterotrophic bacteria in this ecosystem. Collectively, these studies shed light into the composition of the labile dissolved organic carbon pool and its utilization by heterotrophic bacteria in the surface ocean.