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，尽管缺乏专门的隔间来容纳微生物群（例如动物肠），但仍依靠微生物群落生存。微生物群落已被广泛证明受益于硅藻排泄物，该排泄物聚集在浮游植物细胞（称为浮游层）周围的微环境中。但是，使硅藻和其他单细胞真核生物通过培养有益细菌并排斥有害细菌来培育特定微生物组的机制尚不清楚。我们假设硅藻的分泌物可能会调节微生物群落，并采用了一种综合性的多组学方法，即使用无处不在的硅藻Asterionellopsis glacialis来揭示其如何调节其自然相关细菌。我们证明了A. glacialis响应细菌重新编程其转录和代谢谱，从而分泌出一组中央代谢物和两种不同寻常的次级代谢物，迷迭香酸和壬二酸。尽管潜在的细菌共生体和机会主义者都利用中枢代谢产物，但迷迭香酸促进有益细菌附着在硅藻上，同时抑制机会主义者的附着。同样，壬二酸可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，但在全球范围内分布在全球海洋中，并且在分类学上仅限于少数细菌属。