Transcriptomic and proteomic responses to very low CO2 suggest multiple carbon concentrating mechanisms in Nannochloropsis oceanica

BackgroundIn industrial oleaginous microalgae such as Nannochloropsis spp., the key components of the carbon concentration mechanism (CCM) machineries are poorly defined, and how they are mobilized to facilitate cellular utilization of inorganic carbon remains elusive.ResultsFor Nannochloropsis oceanica, to unravel genes specifically induced by CO2 depletion which are thus potentially underpinning its CCMs, transcriptome, proteome and metabolome profiles were tracked over 0h, 3h, 6h, 12h and 24h during cellular response from high CO2 level (HC; 50,000ppm) to very low CO2 (VLC; 100ppm). The activity of a biophysical CCM is evidenced based on induction of transcripts encoding a bicarbonate transporter and two carbonic anhydrases under VLC. Moreover, the presence of a potential biochemical CCM is supported by the upregulation of a number of key C4-like pathway enzymes in both protein abundance and enzymatic activity under VLC, consistent with a mitochondria-implicated C4-based CCM. Furthermore, a basal CCM underpinned by VLC-induced upregulation of photorespiration and downregulation of ornithine-citrulline shuttle and the ornithine urea cycles is likely present, which may be responsible for efficient recycling of mitochondrial CO2 for chloroplastic carbon fixation.ConclusionsNannochloropsis oceanica appears to mobilize a comprehensive set of CCMs in response to very low CO2. Its genes induced by the stress are quite distinct from those of Chlamydomonas reinhardtiiandPhaeodactylum tricornutum, suggesting tightly regulated yet rather unique CCMs. These findings can serve the first step toward rational engineering of the CCMs for enhanced carbon fixation and biomass productivity in industrial microalgae.