Herbicide metolachlor alters gene expression and influences the interaction between a bloom-forming cyanobacterium and its chytrid parasite

Metolachlor (MET) is a widely used herbicide, and its extensive application has become a significant source of freshwater pollution. MET not only harms aquatic organisms but can also alter their ecological interactions, such as those between bloom-forming cyanobacteria and their chytrid parasites. Chytrids are zoosporic fungi that naturally regulate cyanobacterial populations. Although it is known that MET affects cyanobacterial metabolism and reduces chytrid fitness, the molecular mechanisms underlying these effects remain largely unknown. Here, we investigate the transcriptional profiles of the toxigenic bloom-forming cyanobacterium Planktothrix agardhii and its obligate chytrid parasite Rhizophydium megarrhizum exposed to an environmentally relevant concentration of MET. We found that MET alters the expression of genes associated with key physiological processes in both organisms. In P. agardhii, it affected genes involved in photosynthesis, gas vesicle synthesis and membrane stability. In R. megarrhizum, it influenced genes related to flagella assembly, developmental transitions and secondary metabolite production. Moreover, the distinct expression pattern observed under combined MET exposure and chytrid infection suggests a synergistic effect on the cyanobacterial host. By impairing chytrid-mediated control of cyanobacteria, MET may allow cyanobacteria to overgrow, thereby promoting bloom formation. This is the first study to uncover the genetic basis of herbicide-induced changes in cyanobacteria-fungal parasite dynamics.