Photophysiological and transcriptomic response to the broad-spectrum herbicides atrazine and glyphosate in a photosynthetic picoeukaryote

To feed the growing global population, intensive agriculture relies on herbicides to maximize productivity, but these come with broad-reaching environmental impacts, particularly deleterious effects on ecosystems through water run-off systems. Picoeukaryotes, with minimal genomes, can be employed to model the modes of action of herbicides on off-target species in the environment. Picochlorum sp. SENEW3 (P. SENEW3) is a poikilohaline green alga and serves as a useful model picoeukaryote due to its small genome and robust growth characteristics. Here, we examined the growth, photophysiological and transcriptomic responses of P. SENEW3 to sublethal concentrations of two common herbicides: atrazine and glyphosate. Atrazine treatment resulted in significant (P<0.0001) reductions in mean photosynthetic maximum yield (F_v/F_m) of 46% and an increase in fluorescence minimum (F_o) of 83%, while glyphosate treatment resulted in a significant (P<0.0001) 30% mean reduction in fluorescence maximum (F_m). Atrazine treatment resulted in significant transcriptomic changes (P<0.01, 1.5 log2 fold change ratio), with increased transcription of 18 genes largely involved in gene expression and ribosomal subunits, carotenoid biosynthesis, carbon fixation and reduced transcription of 27 genes largely related to DNA replication and cell cycle. Treatment with glyphosate resulted in increased transcript abundance of 45 genes, most notably those related to energy generation and redox, and chloroplastic non-photochemical quenching and reduced transcription of 188 genes, largely involved in aa and protein synthesis. Both herbicides resulted in a reduced abundance of transcripts for a nitrogen assimilation cluster. These results highlight the potential for commonly used herbicides to have adverse effects on coastal primary producers and demonstrate the value of P. SENEW3 as a robust model for evaluating the impacts of horticultural compounds and agricultural practices on this ecologically important group of organisms.