Thalassiosira pseudonana growth phase determines gene expression and algicidal behavior of a new Alteromonas...

Phytoplankton-bacterium interactions are pivotal in marine ecosystems, influencing primary production and biogeochemical cycles. Diatoms, in particular, engage in diverse relationships with bacteria, ranging from mutualism to pathogenicity. However, the mechanisms governing the shift between these interactions and how they are shaped by host physiology and environmental context remain unclear. To address this, we investigated how the growth phase of the model diatom Thalassiosira pseudonana influences the behavior of an Alteromonas macleodii strain isolated from the Equatorial Pacific. We find that A. macleodii EP displays a differential algicidal impact on T. pseudonana, depending on the growth phase of the diatom, with the greatest effect occurring during the stationary phase. The algicidal effect can be amplified to impact all growth phases by the addition of an external organic carbon source to the co-cultures. Transcriptomic analysis revealed that A. macleodii EP shifts from motility-associated to growth-associated gene expression patterns in response to the diatom's growth phase and co-culture duration. Bacterial cell-free exudate growth assays and fluorescence microscopy of co-cultures show a two-stage interaction model: initial bacterial swimming and exudate secretion induce diatom death, followed by bacterial aggregation around diatom debris. Comparative transcriptomics of A. macleodii with other algal hosts highlights host-specific bacterial responses, underscoring the context-dependent nature of these interactions. Together, these findings reveal how bacterial behavior and gene expression are modulated by host state and environmental cues, providing a molecular basis for the dynamic roles of diatom-bacterium interactions in shaping microbial community structure.IMPORTANCEDiatoms are responsible for almost a quarter of global primary production, and their ecological roles are shaped by interactions with heterotrophic bacteria. These relationships can range from mutualistic to algicidal, with consequences for nutrient cycling and carbon export. Here, we show that the growth phase of the model diatom Thalassiosira pseudonana shapes its interaction with a newly isolated open-ocean strain of Alteromonas macleodii. Using transcriptomics and co-culture experiments, we demonstrate that bacterial gene expression dynamically shifts with host physiology, transitioning from motility and algicidal activity to aggregation and nutrient acquisition. Our findings reveal a two-stage interaction dynamic and highlight diatom growth phase as a critical, yet often overlooked, factor in determining the outcome of bacteria-algae interactions. By linking host physiology to bacterial behavioral shifts, this study provides new insights into how microscale dynamics can scale up to influence ocean productivity and biogeochemical cycling.