Unicellular eukaryotic phytoplankton, such as diatoms, rely on microbial communities for survival despite lacking specialized compartments to house microbiomes (e.g., animal gut). Microbial communities have been widely shown to benefit from diatom excretions that accumulate within the microenvironment surrounding phytoplankton cells, known as the phycosphere. However, mechanisms that enable diatoms and other unicellular eukaryotes to nurture specific microbiomes by fostering beneficial bacteria and repelling harmful ones are mostly unknown. We hypothesized that diatom exudates may tune microbial communities and employed an integrated multiomics approach using the ubiquitous diatom Asterionellopsis glacialis to reveal how it modulates its naturally associated bacteria. We show that A. glacialis reprograms its transcriptional and metabolic profiles in response to bacteria to secrete a suite of central metabolites and two unusual secondary metabolites, rosmarinic acid and azelaic acid. While central metabolites are utilized by potential bacterial symbionts and opportunists alike, rosmarinic acid promotes attachment of beneficial bacteria to the diatom and simultaneously suppresses the attachment of opportunists. Similarly, azelaic acid enhances growth of beneficial bacteria while simultaneously inhibiting growth of opportunistic ones. We further show that the bacterial response to azelaic acid is numerically rare but globally distributed in the world’s oceans and taxonomically restricted to a handful of bacterial genera. Our results demonstrate the innate ability of an important unicellular eukaryotic group to modulate select bacteria in their microbial consortia, similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely across different bacterial populations.

单细胞真核浮游植物（例如硅藻）依赖微生物群落生存，尽管缺乏专门的隔室来容纳微生物组（例如动物肠道）。微生物群落已被广泛证明受益于硅藻排泄物，这些排泄物积聚在浮游植物细胞周围的微环境（称为藻圈）内。然而，硅藻和其他单细胞真核生物通过培养有益细菌和排斥有害细菌来培育特定微生物组的机制大多未知。我们假设硅藻分泌物可以调节微生物群落，并采用综合多组学方法，利用无处不在的硅藻Asterionellopsis glacialis来揭示它如何调节其自然相关的细菌。我们发现， A. glacialis会根据细菌的反应重新编程其转录和代谢特征，从而分泌一系列中心代谢物和两种不寻常的次级代谢物：迷迭香酸和壬二酸。虽然中心代谢物被潜在的细菌共生体和机会主义者利用，但迷迭香酸促进有益细菌附着到硅藻上，同时抑制机会主义者的附着。同样，壬二酸可以促进有益细菌的生长，同时抑制机会性细菌的生长。我们进一步表明，细菌对壬二酸的反应在数量上很少见，但分布在世界各地的海洋中，并且在分类学上仅限于少数细菌属。 我们的结果证明了一个重要的单细胞真核生物群具有调节微生物群落中选定细菌的先天能力，类似于高等真核生物，使用独特的次级代谢产物来调节不同细菌群体的细菌生长和行为。