The CO2-Concentrating Mechanism and Carbon Assimilation

doi:10.1016/B978-0-12-370873-1.00016-2

The Chlamydomonas Sourcebook (Second Edition)

Volume 2, 2009, Pages 257-301

https://doi.org/10.1016/B978-0-12-370873-1.00016-2 Get rights and content

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This chapter discusses CO2 concentrating mechanisms.Photosynthetic carbon metabolism, photorespiratory metabolism, and acetate metabolism are described to emphasize the metabolism of carbon assimilation. CCMs represent an evolutionary adaptation acquired by microalgae and cyanobacteria in response to increased O2 and decreased CO2 availability, especially in aquatic environments. Photosynthetic organisms absorb CO2 as the major substrate to support photosynthesis, the beginning of energy flow into living organisms and one of the primary processes comprising the global carbon cycle. Therefore, changes in CO2 concentrations can have a profound impact on photosynthesis and many related processes in carbon metabolism, which subsequently influence the biotic environment of earth. In addition to a variable supply from respiratory sources, equilibration of CO2 between aqueous environments and the atmosphere is relatively slow, which can result in a depletion of the aqueous CO2 during active photosynthesis. Adding a further challenge, the roughly 104-fold slower diffusion of CO2 in water versus air greatly exacerbates the problem of CO2 supply to Rubisco.

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Cited by (37)

Environmental and nuclear influences on microalgal chloroplast gene expression
2023, Trends in Plant Science
Microalgal chloroplasts, such as those of the model organism Chlamydomonas reinhardtii, are emerging as a new platform to produce recombinant proteins, including industrial enzymes, diagnostics, as well as animal and human therapeutics. Improving transgene expression and final recombinant protein yields, at laboratory and industrial scales, require optimization of both environmental and cellular factors. Most studies on C. reinhardtii have focused on optimization of cellular factors. Here, we review the regulatory influences of environmental factors, including light (cycle time, intensity, and quality), carbon source (CO₂ and organic), and temperature. In particular, we summarize their influence via the redox state, cis-elements, and trans-factors on biomass and recombinant protein production to support the advancement of emerging large-scale light-driven biotechnology applications.
Urea as a source of nitrogen and carbon leads to increased photosynthesis rates in Chlamydomonas reinhardtii under mixotrophy
2023, Journal of Biotechnology
Microalgae is a potential source of bioproducts, including feedstock to biofuels. Urea has been pointed as potential N source for microalgae growth. Considering that urea metabolism releases HCO₃^- to the medium, we tested the hypothesis that this carbon source could improve photosynthesis and consequently growth rates of Chlamydomonas reinhardtii. In this sense, the metabolic responses of C. reinhardtii grown with ammonium and urea as nitrogen sources under mixotrophic and autotrophic conditions were investigated. Overall, the mixotrophy led to increased cell growth as well as to a higher accumulation of lipids independent of N source, followed by a decrease in photosynthesis over the growth phases. In mixotrophy, urea stimulates growth in terms of cell number and dry weight. Furthermore, higher photosynthesis was verified in late logarithmic phase compared to ammonium. Under autotrophy conditions, although cell number and biomass were reduced, there was higher production of starch independent of N source. Nonetheless, urea-based autotrophic treatments stimulated biomass production compared to ammonium-based treatment. Under mixotrophy higher input of carbon into the cell from acetate and urea optimized photosynthesis and consequently promoted cell growth. Together, these results suggest urea as alternative source of carbon, improving photosynthesis and cell growth in C. reinhardtii.
Nuclear proteome analysis of Chlamydomonas with response to CO<inf>2</inf> limitation
2020, Algal Research
Citation Excerpt :
Protein identification and quantification were performed using two different mass spectrometric techniques to achieve a deep and robust characterization of changes in protein expression related to acclimation to LCO2. It is well established that a CO2 concentration of 0.04% in air causes rapid CCM induction along with up-regulation of several genes encoding key CCM proteins including carbonic anhydrases (CAs), putative Ci transporters, and other LCO2 inducible (LCI) proteins [52]. Among these genes, LCO2-inducible membrane protein (LCI; Cre03.g162800), anion transporter (LCIA/NAR1.2; Cre06.g309000), LCO2-inducible chloroplast envelope protein (CCP1; Cre04.g223300 and CCP2; Cre04.g222750), ABC transporter (HLA3; Cre02.g097800), mitochondrial carbonic anhydrase beta type (CAH4; Cre05.g248400), mitochondrial carbonic anhydrase (CAH5; Cre05.g248450) have been previously shown to be rapidly up-regulated under LCO2 conditions [21,24,53,54], with rapid increases in expression after only 1 h of exposure to LCO2 conditions.
Chlamydomonas reinhardtii is a unicellular green alga that can survive at a wide range of inorganic carbon (Ci) concentrations by regulating the activity of a CO₂-concentrating mechanism (CCM) as well as other cellular functions. Under CO₂ limited conditions, C. reinhardtii cells display a wide range of adaptive responses including changes in photosynthetic electron transport, mitochondria localization in the cells, the structure of the pyrenoid starch sheath, and primary metabolism. In addition to these functional and structural changes, gene and protein expression are also affected. Several physiological aspects of the CO₂ response mechanism have been studied in detail. However, the regulatory components (transcription factors and transcriptional regulators) involved in this process are not fully characterized. Here we report a comprehensive analysis of the C. reinhardtii nuclear proteome using liquid chromatography electrospray ionization spectrometry (LC-ESI-MS). The study aims to identify the proteins that govern adaptation to varying CO₂ concentrations in Chlamydomonas. The nuclear proteome of C. reinhardtii cells grown in the air at high (5%) and low (0.04%) CO₂ concentrations were analyzed. Using this approach, we identified 1378 proteins in total, including 90 putative transcription factors and 27 transcriptional regulators. Characterization of these new regulatory components could shed light on the molecular mechanisms underlying acclimation to CO₂ stress.
The influence of exogenous organic carbon assimilation and photoperiod on the carbon and lipid metabolism of Chlamydomonas reinhardtii
2018, Algal Research
Citation Excerpt :
C. reinhardtii contains multiple copies of these genes with different putative localisations. Consequently it is assumed that acetyl-CoA is synthesised from acetate in multiple organelles [18] (Fig. 1). Previous studies have demonstrated that increasing the concentration of exogenous acetate leads to a proportionate increase in TAG (up to 50 mM acetate) [19,20].
Microalgae are a promising platform for the production of renewable fuels and oleochemicals. Despite significant research efforts to understand the mechanisms of algal lipid accumulation, the influence of commercially relevant growth conditions on the lipid metabolism is poorly understood. To characterise the impact of differing organic carbon availabilities and photoperiod on the response of the model alga Chlamydomonas reinhardtii to nitrogen stress, the expression of key genes involved in the central carbon metabolism were monitored over a time-course of nitrogen deprivation. In addition, the growth, PSII integrity, chlorophyll content, triacylglycerol (TAG) content, starch content, and fatty acid composition were characterised. Results indicate that both organic carbon availability and photoperiod regulate the lipid accumulation response of C. reinhardtii. Under mixotrophic conditions, organic carbon uptake is favoured over photosynthesis, transcript abundance of lipid synthesis genes rapidly increase and acetate is funnelled to TAG synthesis. In contrast, autotrophic cultures lacking organic carbon experienced a slower rate of photosynthetic degradation and funnelled the majority of sequestered carbon to starch synthesis. Dark periods induced catabolism of both starch and TAG in autotrophic cultures but TAG alone in mixotrophic cultures. Furthermore, diurnal light enhanced starch synthesis under mixotrophic conditions. Finally, transcript analysis indicated that PGD1, important for the routing of oleic acid to TAG, was reliant on organic carbon availability, resulting in reduced C18:1 fatty acid accumulation in autotrophic cultures.
A novel activation domain is essential for CIA5-mediated gene regulation in response to CO<inf>2</inf> changes in Chlamydomonas reinhardtii
2017, Algal Research
Citation Excerpt :
This mutant can grow under high CO2 and grows more slowly than the wild type in low CO2. However, it cannot grow in very low CO2 (i.e., < 100 ppm) and appears to completely lack the changes in gene expression associated with acclimation to low CO2 [15]. Further studies show that almost all identified Low CO2 Inducible (LCI) genes remain unchanged when cia5 mutant is exposed to limiting CO2 [14–18].
The inducible CO₂ concentrating mechanism (CCM) of microalgae is essential for their acclimation to highly variable aquatic inorganic carbon levels. The key transcriptional regulator, CIA5, affects expression of thousands of genes in Chlamydomonas reinhardtii, but the molecular characteristics of this important protein are poorly understood. This study identifies a functional activation domain in CIA5 and demonstrates the functionality of a mini-CIA5 including only the zinc-binding domain and the identified activation domain. A highly conserved 130aa region from CIA5 exhibits auto-activation in yeast and appears responsible for the markedly slow migration of CIA5 when analyzed by SDS-PAGE. This 130aa region or either half of this region also effectively replaced the activation domain of a modified designer Transcription Activator-like Element (dTALE) in targeted activation of an endogenous Chlamydomonas gene. Additionally, a mini-CIA5 combining the conserved zinc-binding domain with the 130aa putative activation domain complemented the growth phenotype of the cia5 mutant and triggered CO₂-regulated gene expression patterns similar to wild-type cells or cia5 complemented with the full-length CIA5. Although the mini-CIA5 complementation did not fully restore wild-type growth rates or full gene induction/repression amplitudes, especially in very low CO₂, this newly identified activation domain combined with the previously described zinc-binding domain are demonstrated to be the key essential components of CIA5 that permit rapid CIA5-mediated responses to changes in CO₂ concentrations.
Ions channels/transporters and chloroplast regulation
2015, Cell Calcium
Ions play fundamental roles in all living cells and their gradients are often essential to fuel transports, to regulate enzyme activities and to transduce energy within and between cells. Their homeostasis is therefore an essential component of the cell metabolism. Ions must be imported from the extracellular matrix to their final subcellular compartments. Among them, the chloroplast is a particularly interesting example because there, ions not only modulate enzyme activities, but also mediate ATP synthesis and actively participate in the building of the photosynthetic structures by promoting membrane-membrane interaction. In this review, we first provide a comprehensive view of the different machineries involved in ion trafficking and homeostasis in the chloroplast, and then discuss peculiar functions exerted by ions in the frame of photochemical conversion of absorbed light energy.

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Chapter 8 - The CO2-Concentrating Mechanism and Carbon Assimilation

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Chapter 8 - The CO₂-Concentrating Mechanism and Carbon Assimilation