From partners to pathogens: Metabolic duality in algal-bacterial interactions

Interactions between phytoplankton and bacteria are often classified as beneficial or harmful, yet interactions between the same partners can shift between these states. Here, we examine bacterial pathogenicity toward marine phytoplankton, focusing on how algal-bacterial interactions become harmful. In several Roseobacter-phytoplankton systems, bacteria repurpose metabolites produced or exchanged during the interaction by altering their concentration, signaling function, or metabolic fate, thereby contributing to host damage. We define this context-dependent repurposing as metabolic duality. We contrast this strategy with algicidal activity that does not require a demonstrated prior interaction with the algal partner or an algal-derived substrate. Examples include secreted proteases and small-molecule algicides that bacteria can produce independently of host-derived metabolites. Despite their different mechanisms, these routes often converge on oxidative stress and programmed cell death-like responses in the algal host. Bacterial identity alone does not determine the outcome. Host physiological state, microbial community composition, temperature, nutrients, and the chemical environment can all shift an interaction toward or away from pathogenicity. We therefore propose that phytoplankton pathogenicity is best viewed as an emergent property of the interactions among the bacterium, host, community, and environment. This perspective shifts the central question from which bacteria are pathogens to what makes an interaction pathogenic and provides a framework for understanding when and why algal-bacterial interactions become harmful in the ocean.