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 availability scenarios, transcriptomic analyses revealed altered expression of transfer RNA modification enzymes and biased codon usage of transcripts more abundant during phosphate-limiting versus phosphate-replete conditions, consistent with the role of transfer RNA modifications in regulating codon recognition. To associate the observed shift in the expression of the transfer RNA modification enzyme complement with the transfer RNAs encoded by M. commoda, we also determined the transfer RNA 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 phosphate 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 transfer RNA 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 downregulated protein-encoding genes to the cell biological controls that underpin acclimation to changing environmental conditions.

Department of Mathematics and Statistics Dalhousie University Halifax Nova Scotia B3H 4R2 CA

Institute of Parasitology Biology Centre Czech Academy of Sciences 370 05 České Budějovice

Joint Genome Institute Lawrence Berkeley National Laboratory Berkeley CA 94720 USA

Josephine Bay Paul Center for Comparative Molecular Biology and Evolution Marine Biological Laboratory Woods Hole MA 02543 USA

Max Planck Institute for Evolutionary Biology 24306 Plön DE

Ocean EcoSystems Biology Unit RD3 GEOMAR Helmholtz Centre for Ocean Research 24148 Kiel DE

Ocean Sciences Department University of California Santa Cruz Santa Cruz CA 95064 USA

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