Abstract
Carbon-concentrating mechanisms (CCMs) enable efficient photosynthesis and growth in CO2-limiting environments, and in eukaryotic microalgae localisation of Rubisco to a microcompartment called the pyrenoid is key. In the model green alga Chlamydomonas reinhardtii, Rubisco preferentially relocalises to the pyrenoid during CCM induction and pyrenoid-less mutants lack a functioning CCM and grow very poorly at low CO2. The aim of this study was to investigate the CO2 response of pyrenoid-positive (pyr+) and pyrenoid-negative (pyr-) mutant strains to determine the effect of pyrenoid absence on CCM induction and gene expression. Shotgun proteomic analysis of low-CO2-adapted strains showed reduced accumulation of some CCM-related proteins, suggesting that pyr- has limited capacity to respond to low-CO2 conditions. Comparisons between gene transcription and protein expression revealed potential regulatory interactions, since Rubisco protein linker (EPYC1) protein did not accumulate in pyr- despite increased transcription, while elements of the LCIB/LCIC complex were also differentially expressed. Furthermore, pyr- showed altered abundance of a number of proteins involved in primary metabolism, perhaps due to the failure to adapt to low CO2. This work highlights two-way regulation between CCM induction and pyrenoid formation, and provides novel candidates for future studies of pyrenoid assembly and CCM function.
Highlights
Upon exposure to low CO2, most unicellular eukaryotic algae are able to induce a carbon-concentrating mechanism (CCM), which generally includes a series of inorganic carbon transporters and carbonic anhydrases that deliver high concentrations of CO2 to the primary photosynthetic carboxylase Rubisco (Reinfelder, 2011)
Genome-wide high-throughput transcriptome studies (Miura et al, 2004; Brueggeman et al, 2012; Fang et al, 2012) have since helped to identify novel low-CO2-responsive genes, some of which form an integral part of the Chlamydomonas CCM model—for example, the chloroplast membrane transporter low-CO2-inducible A protein (LCIA) and the peri-pyrenoidal protein LCIB that may be involved in CO2 re/capture (Jin et al, 2016)
These studies quantified the extent of genetic remodelling microalgae undergo when acclimating to low CO2 and provided key evidence that the Chlamydomonas CCM is under the high-level regulation of a nuclear factor, CIA5
Summary
Upon exposure to low CO2, most unicellular eukaryotic algae are able to induce a carbon-concentrating mechanism (CCM), which generally includes a series of inorganic carbon transporters and carbonic anhydrases that deliver high concentrations of CO2 to the primary photosynthetic carboxylase Rubisco (Reinfelder, 2011). Genome-wide high-throughput transcriptome studies (Miura et al, 2004; Brueggeman et al, 2012; Fang et al, 2012) have since helped to identify novel low-CO2-responsive genes, some of which form an integral part of the Chlamydomonas CCM model—for example, the chloroplast membrane transporter low-CO2-inducible A protein (LCIA) and the peri-pyrenoidal protein LCIB that may be involved in CO2 re/capture (Jin et al, 2016) These studies quantified the extent of genetic remodelling microalgae undergo when acclimating to low CO2 and provided key evidence that the Chlamydomonas CCM is under the high-level regulation of a nuclear factor, CIA5 ( known as CCM1). Studies that compare wildtype and high-CO2-requiring mutants under contrasting growth conditions (high CO2 for CCM-repressed and low CO2 for CCM-induced), coupled to high-throughput tools capable of resolving complex biological samples, provide a powerful tool to advance our understanding of the algal CCM
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