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

Li Wei,Chen Shen,Wenxu Zhou,Ansgar Poetsch,Xiaoyan Jing,Yandu Lu,Mohamed El Hajjami,Jian Xu,Qiang Hu,Wuxin You,Jing Li

doi:10.1186/s13068-019-1506-8

Abstract

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 0 h, 3 h, 6 h, 12 h and 24 h during cellular response from high CO2 level (HC; 50,000 ppm) to very low CO2 (VLC; 100 ppm). 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 reinhardtii and Phaeodactylum 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.

Highlights

Elevated atmospheric CO2 levels, one consequence of fossil fuel use and deforestation, are leading to global warming and oceanic acidification
As a feat of plant evolution driven by gradual reduction in atmosphere C O2 concentration, concentration mechanism (CCM) act as a dissolved inorganic carbon (DIC) pump to increase CO2 concentration in the vicinity of RuBisCO [9]
In the biochemical CCM, HCO3− is converted into oxaloacetate by phosphoenolpyruvate carboxylase (PEPC), which is decarboxylated into C O2 and malate by malate dehydrogenase (MDH) and/or malic enzyme (ME); the CO2 enters the Calvin cycle [9, 11, 13]

Summary

Introduction

Elevated atmospheric CO2 levels, one consequence of fossil fuel use and deforestation, are leading to global warming and oceanic acidification. The inadequate productivity of microalgal biomass and oil, at both ambient (air level; 0.04% v/v) and elevated (flue gas level; usually > 5% v/v) CO2 concentrations [5, 6], has severely hindered the efforts to fulfill these promises [7] To tackle this challenge, mechanistic insights into substrate intake machineries of these industrial oleaginous microalgae, in particular carbon concentrating mechanisms (CCMs; [8]), are essential. In the basal CCM, mitochondrial γ-type CAs and NADH–ubiquinone oxidoreductase complex I of the respiratory chain recycle mitochondrial C O2 for the carbon fixation in chloroplasts and reduce the leakage of CO2 from plant cells (e.g., Arabidopsis; [14]) Despite these important roles, activities of these CCMs are all highly regulated in the cell. In 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

Methods

Results

Conclusion