Marine bacteria-phytoplankton interaction ultimately shapes ecosystem productivity. The biochemical mechanisms underlying their interactions become increasingly known, yet how these ubiquitous interactions drive bacterial evolution has not been illustrated. Here, we sequenced genomes of 294 bacterial isolates associated with 19 coexisting diatom cells. These bacteria constitute eight genetically monomorphic populations of the globally abundant Roseobacter group. Six of these populations are

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... ers of Sulfitobacter, arguably the most prevalent bacteria associated with marine diatoms. A key finding is that populations varying at the intra-specific level have been differentiated and each are either associated with a single diatom host or with multiple hosts not overlapping with those of other populations. These closely related populations further show functional differentiation; they differ in motility phenotype and they harbor distinct types of secretion systems with implication for mediating organismal interactions. This interesting host-dependent population structure is even evident for demes within a genetically monomorphic population but each associated with a distinct diatom cell, as shown by a greater similarity in genome content between isolates from the same host compared to those from different hosts. Importantly, the intra- and inter-population differentiation pattern remains when the analyses are restricted to isolates from intra-specific diatom hosts, ruling out distinct selective pressures and instead suggesting coexisting microalgal cells as physical barriers of bacterial gene flow. Taken together, microalgae-associated bacteria display a unique microscale metapopulation structure, which consists of numerous small populations whose evolution is driven by random genetic drift.