Dissecting nitrogen starvation signaling in Chlamydomonas: Insights from arginine-fed transcriptome profiling

Abstract

Nitrogen (N) acquisition from environmental sources is critical for most organisms. In plants and other photosynthetic eukaryotes, the limitation of available N induces global changes in gene expression; yet, the underlying regulatory mechanisms remain largely unknown. Chlamydomonas reinhardtii primarily utilizes inorganic N sources but also thrives on organic N sources like arginine. Our recent characterization of the molecular and physiological responses of arginine-fed Chlamydomonas cultures reveals a stark resemblance to the responses invoked by N starvation. To determine if arginine feeding triggers full-scale N starvation responses in the absence of metabolic N limitation, we compared the transcriptomes of arginine-fed cultures with those of early and late stages of N starvation. Our analysis shows that arginine-fed cells maintain both the N starvation-induced upregulation of N scavenging genes and genome-wide downregulation of genes involved in energy-producing carbon flow during exponential growth. Our study defines the N starvation-triggered gene regulatory network in two tiers: the early response involves N scavenging within the first two hours, and the late response includes the rerouting of energy-producing carbon flow into the biosynthesis of energy storage molecules. This regulation operates independently of growth, allowing cells to balance N and carbon budgets regardless of growth status. Our findings pave the way for future research on the triggers of N starvation responses in photosynthetic eukaryotic organisms and the strategies to enhance the production of starvation-associated high-value products in microalgae.