scholarly journals Alternative electron pathways of photosynthesis drive the algal CO2 concentrating mechanism

2021 ◽  
Author(s):  
Adrien Burlacot ◽  
Ousmane Dao ◽  
Pascaline Auroy ◽  
Stephan Cuiné ◽  
Yonghua Li-Beisson ◽  
...  
Keyword(s):  
Inorganic Carbon ◽  
Electron Flow ◽  
Crop Productivity ◽  
Anthropogenic Emissions ◽  
Chlorophyll Fluorescence Parameter ◽  
Concentrating Mechanism ◽  
Fluorescence Parameter ◽  
Algal Photosynthesis ◽  
Cellular Components ◽  
The Way

AbstractGlobal photosynthesis consumes ten times more CO2 than net anthropogenic emissions, and microalgae account for nearly half of this consumption1. The great efficiency of algal photosynthesis relies on a mechanism concentrating CO2 (CCM) at the catalytic site of the carboxylating enzyme RuBisCO, thus enhancing CO2 fixation2. While many cellular components involved in the transport and sequestration of inorganic carbon (Ci) have been uncovered3,4, the way microalgae supply energy to concentrate CO2 against a thermodynamic gradient remains elusive4-6. Here, by monitoring dissolved CO2 consumption, unidirectional O2 exchange and the chlorophyll fluorescence parameter NPQ in the green alga Chlamydomonas, we show that the complementary effects of cyclic electron flow and O2 photoreduction, respectively mediated by PGRL1 and flavodiiron proteins, generate the proton motive force (pmf) required by Ci transport across thylakoid membranes. We demonstrate that the trans-thylakoid pmf is used by bestrophin-like Ci transporters and further establish that a chloroplast-to-mitochondria electron flow contributes to energize non-thylakoid Ci transporters, most likely by supplying ATP. We propose an integrated view of the CCM energy supply network, describing how algal cells distribute photosynthesis energy to power different Ci transporters, thus paving the way to the transfer of a functional algal CCM in plants towards improving crop productivity.One sentence summaryPhotosynthetic alternative electron flows and mitochondrial respiration drive the algal CO2 concentrating mechanism

Adaptation of a Chlamydomonas mutant with reduced rate of photorespiration to different concentrations of CO2

2005 ◽  
Vol 83 (7) ◽  
pp. 834-841 ◽  
Author(s):  
Kensaku Suzuki ◽  
Hidenori Onodera
Keyword(s):  
Chlorophyll Fluorescence ◽  
Chlamydomonas Reinhardtii ◽  
Inorganic Carbon ◽  
Electron Flow ◽  
Effective Quantum Yield ◽  
Wild Type ◽  
Chlorophyll Fluorescence Parameters ◽  
Phosphoglycolate Phosphatase ◽  
Concentrating Mechanism ◽  
Type Strains

It has been widely accepted that Chlamydomonas reinhardtii cells utilize inorganic carbon very efficiently for photosynthesis by operating a CO2-concentrating mechanism (CCM) under conditions of limited CO2. To help define the mechanism, 7FR2N, one of the suppressor double mutants of phosphoglycolate phosphatase-deficient (pgp1) mutants that have a reduced photorespiration rate (RPR) was crossed with wild-type strains to generate the strain N21 as a single RPR mutant. The comparison of photosynthetic characteristics with wild-type strains after the cells adapted to different concentrations of CO2 revealed that photosynthetic affinity for inorganic carbon was higher than that in wild-type strains after adaptation to concentrations between 50 µL·L–1 CO2 and 5% CO2. Chlorophyll fluorescence parameters were also compared, and the biggest difference between N21 and the wild-type strains was observed in the photochemical quenching and effective quantum yield of photosystem II (ΔF/Fm′) at the CO2 compensation point. These values in N21 increased in a similar manner to the photosynthetic affinity for CO2, and increased significantly when the cells adapted to low-CO2 levels, whereas the values in the wild-type strains were apparently lower without any significant changes, regardless of the CO2 concentrations to which they were adapted. Although it was not clear if a nonphotochemical quenching parameter (NPQ) in N21 was higher than that in wild-type strains, NPQ increased coincidentally with the increase in photosynthetic affinity for inorganic carbon when the CO2 concentrations to which the strains were adapted decreased, in both the mutant and wild-type strain, suggesting that this form of NPQ reflects the operation of CCM in certain conditions. Possible candidates for the RPR mutation and the relationship between CCM and photosynthetic electron flow are discussed.Key words: Chlamydomonas reinhardtii, chlorophyll fluorescence, CO2-concentrating mechanism, low-CO2 responsive gene, phosphoglycolate phosphatase, photorespiration.

Modulation of photosynthesis and inorganic carbon acquisition in a marine microalga by nitrogen, iron, and light availability

2005 ◽  
Vol 83 (7) ◽  
pp. 917-928 ◽  
Author(s):  
Erica B Young ◽  
John Beardall
Keyword(s):  
Inorganic Carbon ◽  
Dunaliella Tertiolecta ◽  
Initial Slope ◽  
Carbon Concentrating Mechanism ◽  
High Affinity ◽  
N Limitation ◽  
Marine Microalga ◽  
Concentrating Mechanism ◽  
Energy Limitation ◽  
Use Efficiency

The marine microalga Dunaliella tertiolecta Butcher expresses a high affinity for dissolved inorganic carbon (DIC) through a carbon-concentrating mechanism (CCM), known to be influenced by CO2 availability and instantaneous light supply. However, the regulation by light and nutrient supply during growth is less understood, although N and Fe limitation impose an energy limitation by compromising the photosynthetic apparatus. Dunaliella tertiolecta was grown under steady-state conditions of limited light, N, and Fe availability, and the affinity for DIC was measured under saturating light. High affinity DIC uptake capacity was maintained by D. tertiolecta under all growth-limiting conditions, but was modulated in response to the limiting resource. Affinity of photosynthesis for DIC(k0.5) was significantly reduced in cells grown under low light, both in turbidostats and in batch culture (p ≤ 0.03), although cell-normalized Pmax was not significantly affected. In contrast, N and Fe limitation resulted in a significant reduction in cell chlorophyll, Pmax, and maximum photosystem II quantum yield (Fv/Fm), but the affinity for DIC was enhanced with increasing N or Fe stress. While the affinity for DIC improved with increasing N stress (k0.5 < 17.8 µM at µ = 0.27 d–1 versus k0.5 > 26 µM at µ ≥ 0.77 d–1), light use efficiency (α) was impaired under N limitation, suggesting a trade-off between light harvesting capacity and active DIC uptake. Stable C isotope analysis of Fe-limited cells confirmed a lower fractionation by the most Fe-limited cells, consistent with the k0.5 data and more active DIC acquisition (δ13C = –19.56 at µ = 0.27 d–1 cf. δ13C = –26.28 at µ = 0.77 d–1). Assessment of affinity for DIC using k0.5 was supported by the close fit of P versus DIC curves to Michaelis–Menten kinetics; with the high DIC affinity of D. tertiolecta, there was poor resolution in the initial slope of the P versus DIC curve as a parameter of affinity for DIC. Enhanced DIC uptake efficiency under Fe and N limitation may relate to improved resource-use efficiency conferred by CCM activity.Key words: algae, carbon-concentrating mechanism, iron, light, nitrogen, nutrient limitation, photosynthesis.

scholarly journals Identification of Two Genes, sll0804 and slr1306, as Putative Components of the CO2-Concentrating Mechanism in the Cyanobacterium Synechocystis sp. Strain PCC 6803

2008 ◽  
Vol 190 (24) ◽  
pp. 8234-8237 ◽  
Author(s):  
Shulu Zhang ◽  
Kevin W. Spann ◽  
Laurie K. Frankel ◽  
James V. Moroney ◽  
Terry M. Bricker
Keyword(s):  
Inorganic Carbon ◽  
Carbon Concentrating Mechanism ◽  
Co2 Concentrating Mechanism ◽  
Concentrating Mechanism ◽  
Synechocystis Sp ◽  
Pcc 6803

ABSTRACT Insertional transposon mutations in the sll0804 and slr1306 genes were found to lead to a loss of optimal photoautotrophy in the cyanobacterium Synechocystis sp. strain PCC 6803 grown under ambient CO2 concentrations (350 ppm). Mutants containing these insertions (4BA2 and 3ZA12, respectively) could grow photoheterotrophically on glucose or photoautotrophically at elevated CO2 concentrations (50,000 ppm). Both of these mutants exhibited an impaired affinity for inorganic carbon. Consequently, the Sll0804 and Slr1306 proteins appear to be putative components of the carbon-concentrating mechanism in Synechocystis sp. strain PCC 6803.

scholarly journals pH determines the energetic efficiency of the cyanobacterial CO2 concentrating mechanism

2016 ◽  
Vol 113 (36) ◽  
pp. E5354-E5362 ◽  
Author(s):  
Niall M. Mangan ◽  
Avi Flamholz ◽  
Rachel D. Hood ◽  
Ron Milo ◽  
David F. Savage
Keyword(s):  
Intracellular Ph ◽  
Inorganic Carbon ◽  
Quantitative Description ◽  
Carbon Accumulation ◽  
Energetic Efficiency ◽  
Ribulose Bisphosphate Carboxylase ◽  
Competitive Reaction ◽  
Bisphosphate Carboxylase ◽  
Concentrating Mechanism ◽  
Ribulose Bisphosphate Carboxylase Oxygenase

Many carbon-fixing bacteria rely on a CO2 concentrating mechanism (CCM) to elevate the CO2 concentration around the carboxylating enzyme ribulose bisphosphate carboxylase/oxygenase (RuBisCO). The CCM is postulated to simultaneously enhance the rate of carboxylation and minimize oxygenation, a competitive reaction with O2 also catalyzed by RuBisCO. To achieve this effect, the CCM combines two features: active transport of inorganic carbon into the cell and colocalization of carbonic anhydrase and RuBisCO inside proteinaceous microcompartments called carboxysomes. Understanding the significance of the various CCM components requires reconciling biochemical intuition with a quantitative description of the system. To this end, we have developed a mathematical model of the CCM to analyze its energetic costs and the inherent intertwining of physiology and pH. We find that intracellular pH greatly affects the cost of inorganic carbon accumulation. At low pH the inorganic carbon pool contains more of the highly cell-permeable H2CO3, necessitating a substantial expenditure of energy on transport to maintain internal inorganic carbon levels. An intracellular pH ≈8 reduces leakage, making the CCM significantly more energetically efficient. This pH prediction coincides well with our measurement of intracellular pH in a model cyanobacterium. We also demonstrate that CO2 retention in the carboxysome is necessary, whereas selective uptake of HCO3− into the carboxysome would not appreciably enhance energetic efficiency. Altogether, integration of pH produces a model that is quantitatively consistent with cyanobacterial physiology, emphasizing that pH cannot be neglected when describing biological systems interacting with inorganic carbon pools.

scholarly journals Condensation of Rubisco into a proto-pyrenoid in higher plant chloroplasts

2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Nicky Atkinson ◽  
Yuwei Mao ◽  
Kher Xing Chan ◽  
Alistair J. McCormick
Keyword(s):  
Chlamydomonas Reinhardtii ◽  
Recent Work ◽  
Single Phase ◽  
Inorganic Carbon ◽  
Higher Plants ◽  
Initial Step ◽  
Operating Efficiency ◽  
Higher Plant ◽  
Spontaneous Condensation ◽  
Concentrating Mechanism

AbstractPhotosynthetic CO2 fixation in plants is limited by the inefficiency of the CO2-assimilating enzyme Rubisco. In most eukaryotic algae, Rubisco aggregates within a microcompartment known as the pyrenoid, in association with a CO2-concentrating mechanism that improves photosynthetic operating efficiency under conditions of low inorganic carbon. Recent work has shown that the pyrenoid matrix is a phase-separated, liquid-like condensate. In the alga Chlamydomonas reinhardtii, condensation is mediated by two components: Rubisco and the linker protein EPYC1 (Essential Pyrenoid Component 1). Here, we show that expression of mature EPYC1 and a plant-algal hybrid Rubisco leads to spontaneous condensation of Rubisco into a single phase-separated compartment in Arabidopsis chloroplasts, with liquid-like properties similar to a pyrenoid matrix. This work represents a significant initial step towards enhancing photosynthesis in higher plants by introducing an algal CO2-concentrating mechanism, which is predicted to significantly increase the efficiency of photosynthetic CO2 uptake.

scholarly journals Elevated Inorganic Carbon Concentrating Mechanism Confers Tolerance to High Light in an Arctic Chlorella sp. ArM0029B

2018 ◽  
Vol 9 ◽  
Author(s):  
Kwon Hwangbo ◽  
Jong-Min Lim ◽  
Seok-Won Jeong ◽  
Jayaraman Vikramathithan ◽  
Youn-Il Park ◽  
...  
Keyword(s):  
Inorganic Carbon ◽  
High Light ◽  
Carbon Concentrating Mechanism ◽  
Chlorella Sp ◽  
Concentrating Mechanism
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