Coastal blue ecosystems are among the most productive on Earth, yet the genomic basis of microbial niche organization along the transition from estuarine to oceanic waters remains poorly resolved, particularly for uncultured lineages. Here, we combined PacBio HiFi long-read metagenomics, targeted single-cell genomics and Illumina short-read metagenomics to investigate subtropical microbial communities in the South China Sea. We recovered 381 genomes, including 279 prokaryotic metagenome-assembled genomes (MAGs) and 102 protistan single-cell or metagenome-assembled genomes (SMAGs). Functional profiling assigned 101 protistan SMAGs to 26 mixotrophs, 45 phototrophs and 30 heterotrophs, supporting trophic strategy as a major axis of genome-level differentiation.

Recruitment of these genomes to 24 monthly samples revealed seasonal succession, with phototrophic protists enriched in winter–spring, prokaryotic MAGs increasing during warmer months and heterotrophic protists becoming more prominent after bloom periods. Spatial recruitment across 146 metagenomes further showed that prokaryotic taxonomy and protistan trophic mode varied along the Pearl River Estuary–South China Sea gradient and were associated with salinity, temperature and pH. Co-occurrence analyses linked these distribution patterns to modular microbial associations. The temporal network contained 174 protist–prokaryote associations organized within seasonal modules, suggesting that cross-domain relationships were coupled to recurrent community succession. In contrast, spatial cross-domain associations were concentrated in a single module linking protistan SMAGs (mostly, diatom Skeletonema) with Bacteroidota, suggesting a spatially structured protist–bacterium association axis. Population-differentiation analyses indicated temporal and/or spatial genetic structure across many SMAGs. In prokaryotes, positively selected genes (pN/pS ≥ 0.8) were associated with nutrient acquisition, extracellular degradation, stress response, transport, regulation and cell-envelope remodeling.

Together, these results provide a genome-resolved view of how trophic strategy, environmental gradients, microbial associations and population differentiation jointly shape the organization of subtropical marine microbial communities along the coastal–oceanic continuum, offering mechanistic insights relevant to the functioning of coastal ecosystems under environmental change.

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