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

Abstract

Metolachlor (MET) is among the most widely used herbicides worldwide and a common freshwater contaminant. Beyond direct toxicity, MET can reshape ecological interactions, including those between bloom-forming cyanobacteria and their chytrid parasites. Although MET is known to reduce chytrid fitness and alter cyanobacterium-chytrid interaction, the molecular basis of these effects remains unknown. Using dual RNA-sequencing, we analysed the gene expression of the toxigenic cyanobacterium Planktothrix agardhii and its obligate chytrid parasite Rhizophydium megarrhizum under exposure to an environmentally relevant concentration of MET. MET reprogrammed the parasite R. megarrhizum by altering the expression of genes governing developmental transitions, xenobiotic stress responses and intracellular signalling in both free-living and infecting cells. The transcriptional signature that typically distinguishes zoospores from infecting chytrids disappeared under MET exposure. This was not due to an arrest of the infection process, but rather to an increase in the baseline expression of infection-associated genes in zoospores, thus blurring the dispersal-to-infection transition. In contrast, P. agardhii showed no transcriptional response to MET in the absence of infection, whereas co-exposure to both the parasite and MET was associated with transcriptional changes related to energy acquisition and carbohydrate metabolism. Overall, our results suggest that MET weakens chytrid top-down control and favours cyanobacterial persistence, with consequences for bloom formation and energy transfer through aquatic trophic webs. Our study provides the first replicated molecular view, using a dual-RNA transcriptomic approach, of how herbicide exposure reshapes the interaction between a bloom-forming cyanobacterium and its chytrid parasite.