Phosphate limitation responses in marine green algae are linked to reprogramming of the tRNA epitranscriptome and codon usage bias.

Marine algae are central to global carbon fixation and their productivity is dictated largely by resource availability. Reduced nutrient availability is predicted for vast oceanic regions as an outcome of climate change, however there is much to learn regarding response mechanisms of the tiny picoplankton that thrive in these environments, especially eukaryotic phytoplankton. Here, we investigate responses of the picoeukaryote Micromonas commoda, a green alga found throughout subtropical and tropical oceans. Under shifting phosphate (P) availability scenarios, transcriptomic analyses revealed altered expression of transfer RNA (tRNA) modification enzymes and biased codon usage of transcripts more abundant during P-limiting versus P-replete conditions, consistent with the role of tRNA modifications in regulating codon recognition. To associate the observed shift in expression of the tRNA modification enzyme complement with the tRNAs encoded by M. commoda, we also determined the tRNA repertoire of this alga revealing potential targets of the modification enzymes. Codon usage bias was particularly pronounced in transcripts encoding proteins with direct roles in managing P-limitation and photosystem-associated proteins that have ill-characterized putative functions in "light stress". The observed codon usage bias corresponds to a proposed stress response mechanism in which the interplay between stress-induced changes in tRNA modifications and skewed codon usage in certain essential response genes drives preferential translation of the encoded proteins. Collectively, we expose a potential underlying mechanism for achieving growth under enhanced nutrient limitation, that extends beyond the catalog of up- or down-regulated protein-encoding genes, to the cell biological controls that underpin acclimation to changing environmental conditions.