Microbial photoautotroph-heterotroph interactions underlie marine food webs and shape ecosystem diversity and structure in upper ocean environments. Here, bacterial community composition, lifestyle preference, and genomic- and proteomic-level metabolic characteristics were investigated for an open ocean ecotype and its associated heterotrophs over 91 days of cocultivation. The associated heterotrophic bacterial assembly mostly constituted five classes, including , , , , and The seven most abundant taxa/genera comprised >90% of the total heterotrophic bacterial community, and five of these displayed distinct lifestyle preferences (free-living or attached) and responses to growth phases. Six high-quality genomes, including and the five dominant heterotrophic bacteria, were reconstructed. The only primary producer of the coculture system, , displayed metabolic processes primarily involved in inorganic nutrient uptake, photosynthesis, and organic matter biosynthesis and release. Two of the flavobacterial populations, and , and an SM1A02 population, displayed preferences for initial degradation of complex compounds and biopolymers, as evinced by high abundances of TonB-dependent transporters (TBDTs), glycoside hydrolase, and peptidase proteins. Polysaccharide utilization loci present in the flavobacterial genomes influence their lifestyle preferences and close associations with phytoplankton. In contrast, the alphaproteobacterium sp. population mainly utilized low-molecular-weight dissolved organic carbon (DOC) through ATP-binding cassette (ABC), tripartite ATP-independent periplasmic (TRAP), and tripartite tricarboxylate transporter (TTT) transport systems. The heterotrophic bacterial populations exhibited complementary mechanisms for degrading derived organic matter and driving nutrient cycling. In addition to nutrient exchange, removal of reactive oxygen species and vitamin trafficking might also contribute to the maintenance of the -heterotroph coculture system and the interactions shaping the system. The high complexity of ecosystems renders it difficult to study marine microbial photoautotroph-heterotroph interactions. Two-member coculture systems of picocyanobacteria and single heterotrophic bacterial strains have been thoroughly investigated. However, interactions comprise far more diverse heterotrophic bacterial associations with single photoautotrophic organisms. In the present study, combined metagenomic and metaproteomic data supplied the metabolic potentials and activities of uncultured dominant bacterial populations in the coculture system. The results of this study shed light on the nature of interactions between photoautotrophs and heterotrophs, improving our understanding of the complexity of environments.