Rapid adaptive evolution of oxylipin-based chemical defense against algicidal bacteria in a bloom-forming diatom.

Phytoplankton, the photosynthetic microalgae driving nearly half of Earth's primary production, are the foundation of marine food webs and central to climate regulation. Skeletonema marinoi is a globally distributed and often dominant diatom species in marine phytoplankton communities. It inhabits a dynamic and frequently hostile microbial environment in which interactions with bacteria can negatively affect its survival. Skeletonema marinoi is susceptible to the algicidal bacterium Kordia algicida that can lyse the algal cells and even terminate entire blooms. The extent to which resistance against such a lysis can evolve in diatoms exposed to biotic stress by algicidal bacteria remains unknown. Using adaptive laboratory evolution, we investigated how S. marinoi adapts to toxins produced by K. algicida. Skeletonema marinoi evolved resistance already after 11 growth cycles under sublethal exposure to algicides. This was accompanied by changes in DNA methylation. Untargeted comparative metabolomics of the original and the evolved population revealed the up-regulation of the oxylipins 5-hydroxyeicosapentaenoic acid, prostaglandin E2, and 17-hydroxydocosahexaenoic acid. These oxylipins significantly inhibited the growth of K. algicida, indicating their role in chemical defense. The metabolic plasticity of diatoms and the rapid evolution observed after exposure to bacteria open new perspectives on our understanding of diatom bloom dynamics in nature.